Time Course of Pathologic Changes in Kidney
Allografts of Positive Crossmatch HLA-Incompatible
Transplant Recipients
Serena M. Bagnasco,
1,4
Andrea A. Zachary,
2
Lorraine C. Racusen,
1
Lois J. Arend,
1
Naima Carter-Monroe,
1
Nada Alachkar,
2
Susanna M. Nazarian,
3
Bonnie E. Lonze,
3
Robert A. Montgomery,
3
and Edward S. Kraus
2
Background. Recipients of incompatible allografts are at increased risk of graft loss. We hypothesized that analysis of
sequential biopsies from these grafts could define progression of graft lesions and identify features predictive of
progression.
Methods. We studied the time course of histologic injury in 745 kidney graft biopsies from 129 patients transplanted with
a positive crossmatch human leukocyte antigenYincompatible kidney between 2000 and 2010 (follow-up of 1Y9 years).
Results. Graft survival was 98% at 1 year and 80% at 5 years after transplantation. Throughout follow-up, 70% of
patients experienced rejection, with 52% showing subclinical rejection in the first year. Cell-mediated rejection was more
frequent than antibody-mediated rejection throughout follow-up. Transplant glomerulopathy (TxGN; cgQ1) developed
in 47% of patients over the period of the study, as early as 3 months in a few patients. TxGN was preceded by glomerulitis
in more than 90% of cases, with a median time interval of 12 months. Glomerulitis and detectable posttransplantation
donor-specific antibodies were risk factors for TxGN (PG0.0001 and PG0.05). C4d-negative antibody-mediated rejection
manifesting as capillaritis (gQ1 and ptcQ1) with detectable donor-specific antibodies was observed in some recipients
(G20%). There was progressively higher average tubulointerstitial scarring (ci+ct) from 3 to 6 to 12 months (PG0.001).
Conclusions. Despite good graft survival, a significant incidence of biopsy-proven rejection occurred in this subset
of closely monitored human leukocyte antigenYincompatible recipients throughout follow-up. Microcirculation in-
flammation, particularly glomerulitis, irrespective of C4d, is associated with a high risk of development of TxGN at 1 year.
Keywords: Kidney, Transplant, Rejection, Glomerulopathy, Antibody-mediated rejection.
(Transplantation 2014;97: 440Y445)
R
ecent progress in the development of desensitization
protocols for recipients with antibodies to donor antigens
has made possible transplantation across human leukocyte
antigen (HLA) and ABO barriers (1Y4). However, recipients
of incompatible allografts remain at risk of harboring per-
sistent donor-specific antibodies (DSA) and developing
antibody-mediated rejection (AMR) after transplantation
(5), with increased risk of graft loss when compared with
compatible transplants (6). As more is known about the
mechanisms of graft injury, defining early and late mor-
phologic manifestations of rejection, particularly antibody-
mediated damage, can offer better insight into the pro-
gression of graft deterioration (7, 8).
The time course in which pathologic changes develop
in living donor recipients undergoing desensitization for
preformed DSA (HLA-incompatible) has not been analyzed
systematically, and often in outcome analyses, correlations
are made using only a single time point for posttransplan-
tation biopsies.
The goal of this study was to define the temporal
manifestation of pathologic changes associated with rejection
and development of chronic injury in serial protocol and in-
dication allograft biopsies in a group of transplant recipients,
Support provided by grant RC1 DK098431 from the National Institute of
Diabetes and Digestive and Kidney Diseases and by the Charles T. Bauer
Foundation (R.A.M.).
Part of the results described in this study were presented in poster format at
the 2012 Renal Week in San Diego, CA, and in platform presentation at
the 2013 USCAP meeting in Baltimore, MD.
1
Department of Pathology, Johns Hopkins University, Baltimore, MD.
2
Department of Medicine, Johns Hopkins University, Baltimore, MD.
3
Department of Surgery, Johns Hopkins University, Baltimore, MD.
4
Address correspondence to: Serena M. Bagnasco, M.D., Department of
Pathology, Johns Hopkins University, Ross 632, 720 Rutland Avenue,
Baltimore, MD 21205.
E-mail: sbagnas1@jhmi.edu
S.M.B. designed the study and wrote the article. A.A.Z. contributed data
and participated in the writing of the article. L.C.R., L.J.A., and N.C.-M.
reviewed the biopsies. N.A., S.M.N., and B.E.L. followed up the patients
and performed the biopsies. R.A.M. contributed to the writing of the
article, performed the transplants, and followed up the patients. E.D.K.
maintained the database and participated in the design and writing of
the article.
Received 26 June 2013. Revision requested 12 July 2013.
Accepted 6 September 2013.
Copyright * 2013 by Lippincott Williams & Wilkins
ISSN: 0041-1337/14/9704-440
DOI: 10.1097/01.TP.0000437177.40551.f4
CLINICAL AND TRANSLATIONAL RESEARCH
440 www.transplantjournal.com Transplantation & Volume 97, Number 4, February 27, 2014
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.