AJR 2000; 175:1417-1422
© American Roentgen Ray Society
Focal Posttransplantation Lymphoproliferative Disorder at the Renal Allograft Hilum
R. Lopez-Ben1,
J. K. Smith1,
C. E. Kew, II2,
P. J. Kenney1,
B. A. Julian2 and
M. L. Robbin1
1
Department of Radiology, The University of Alabama Hospitals, The University
of Alabama at Birmingham, 619 19th St. South, Birmingham, AL 35294.
2
Department of Medicine, Division of Nephrology, The University of Alabama
Hospitals, The University of Alabama at Birmingham, Birmingham, AL
35294.
Received May 6, 1999;
accepted after revision March 21, 2000.
Presented at the annual meeting of the American Roentgen Ray Society, San
Francisco, April-May 1998.
Address correspondence to R. Lopez-Ben.
Abstract
OBJECTIVE. This report describes the imaging characteristics of
focal posttransplantation lymphoproliferative disorder.
CONCLUSION. Posttransplantation lymphoproliferative disorder may be
limited to the allograft. A focal complex mass in the renal allograft hilum
surrounding the main renal blood vessels is a common finding and can be
visualized with sonography. MR imaging can help increase diagnostic
confidence.
Introduction
Posttransplantation lymphoproliferative disorder represents an abnormal
proliferation of B cells in response to either primary or reactivated
infection with Epstein-Barr virus
[1]. This abnormal lymphoid
proliferation occurs in approximately 1% of renal allograft recipients
[2,
3]. The reported imaging
manifestations of posttransplantation lymphoproliferative disorder have
included diffuse adenopathy and single or multiple extranodal masses, usually
within solid organs, which may be distant to the allograft (e.g., liver, lung,
central nervous system, gastrointestinal tract, kidney)
[1,
3]. However, reports suggest
that posttransplantation lymphoproliferative disorder localized to the renal
transplant may be a more frequent manifestation of this disease than
previously recognized [2,
4,5,6,7,8].
Among the renal transplantation patients at our institution, 12 of the 16
patients who had posttransplantation lymphoproliferative disorder during the
past 5 years presented with a mass localized to the renal allograft hilum (the
other four patients presented with multifocal disease). We have recently
described the clinical presentation and outcome of these patients in the
transplantation literature [9].
This report differs from our prior report by describing and illustrating in
greater detail the findings on sonography, CT, and MR imaging. Because of the
nonspecific clinical presentation in these patients, the radiologist should be
familiar with this focal presentation of posttransplantation
lymphoproliferative disorder.
Materials and Methods
A retrospective analysis of our institution's renal transplantation
clinical database from 1993 to 1998 identified 12 patients with a diagnosis of
posttransplantation lymphoproliferative disorder who presented with renal
dysfunction and a renal hilum mass on imaging studies. All patients presented
with worsening renal function during the first year after transplantation. A
more complete description of the clinical presentation of 10 of these patients
has been published recently
[9].
The imaging studies were retrospectively reviewed. Sonographic examinations
were performed using a 4-MHz sector transducer and a 128XP-ART or Sequoia 512
scanner (Acuson, Mountain View, CA). Gray-scale and Doppler settings were
individually optimized. CT was performed with a 9800 HiSpeed scanner (General
Electric Medical Systems, Milwaukee, WI) using standard collimation and table
speed. A 1.5-T Signa scanner (General Electric Medical Systems) was used for
the MR imaging with sequences usually including coronal spin-echo T1-weighted
(TR/TE, 500/20), axial T2-weighted fast spin-echo fat-suppressed (5000/100),
and axial dynamic fast multiplanar spoiled gradient-echo (140/4.2; flip angle,
70°) before and after gadolinium administration (0.2 mg/kg).
Results
Eight patients underwent allograft nephrectomy because of progressive renal
dysfunction, acute rejection due to decreased immunosuppression, or
enlargement of the mass. In the eight patients who underwent allograft
nephrectomy, operative records confirmed the presence of a solid mass in
intimate association with the renal hilar vessels. One patient also presented
with an enlarged lymph node revealed on CT of the pelvis; 1 week later, CT
showed an increase in the number of pelvic nodes and the presence of
retroperitoneal adenopathy in the mid abdomen. A trial of decreased
immunosuppression and antiviral therapy failed in this patient. She underwent
allograft nephrectomy with histopathologic confirmation of posttransplantation
lymphoproliferative disorder, but she later died from progressive disease.
In three of the patients, the mass could not be safely dissected from the
adjacent iliac vessels, thus insufficient tissue was available to make a
definitive diagnosis of posttransplantation lymphoproliferative disorder
histologically. Microscopic examination of the other five nephrectomy
specimens showed a polymorphous infiltrate of large atypical transformed
lymphoid cells within the mass and allograft. Results of flow cytometry and
polymerase chain reaction analysis were consistent with posttransplantation
lymphoproliferative disorder.
Three patients living with functional allografts after reduced maintenance
immunosuppression undergo periodic sonography or CT to monitor the size and
characteristics of the pararenal mass. They have had an average 52% decrease
in the size of the renal hilum mass (mean follow-up time, 19 months). Although
percutaneous biopsy was not performed in these three patients, the decrease in
the mass size after immunosuppression was reduced is clinically consistent
with posttransplantation lymphoproliferative disorder. One patient was lost to
imaging follow-up after reduction of immunosuppression but still has a
functional allograft.
Sonography
In 11 of the 12 patients, sonography was the initial imaging modality and
depicted the mass well (unenhanced CT was the initial examination in one
patient who presented with fever). In 12 patients, we saw a complex hypoechoic
mass adjacent to the renal hilum (Figs.
1A,1B,1C,1D,1E,2A,2B,2C,3A,3B,4A,4B,5A,5B,5C,6A,6B).
The mean diameter of these masses was 4.5 cm. Of interest, perhaps because of
the heightened awareness in our sonography section of this diagnosis, review
of the radiology reports in these cases consistently suggested
posttransplantation lymphoproliferative disorder as a possible cause in the 11
patients who underwent sonography as the initial imaging examination.
View larger version (147K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1A. —37-year-old man with decreasing renal function who was
referred for sonography to exclude hydronephrosis. After immunosuppression was
decreased in patient, mass became markedly smaller and renal function
improved. Longitudinal sonogram of renal transplant shows heterogeneous,
partly cystic mass (cursors) adjacent to renal hilum. Note dilatation
(arrow) of collecting system.
|
|
View larger version (147K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1B. —37-year-old man with decreasing renal function who was
referred for sonography to exclude hydronephrosis. After immunosuppression was
decreased in patient, mass became markedly smaller and renal function
improved. Longitudinal color Doppler sonogram of renal transplant shows main
renal artery (arrow) within hilar mass.
|
|
View larger version (72K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1C. —37-year-old man with decreasing renal function who was
referred for sonography to exclude hydronephrosis. After immunosuppression was
decreased in patient, mass became markedly smaller and renal function
improved. Longitudinal spectral Doppler sonogram of renal transplant shows
right iliac artery before anastomosis with peak systolic velocity of 0.91
m/sec. Corrected angle of insonation slightly exceeds 60°, which may lead
to overestimation of peak systolic velocity.
|
|
View larger version (69K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1D. —37-year-old man with decreasing renal function who was
referred for sonography to exclude hydronephrosis. After immunosuppression was
decreased in patient, mass became markedly smaller and renal function
improved. Longitudinal spectral Doppler sonogram of renal transplant shows
main renal artery (MRA) with peak systolic velocity of 3.10 m/sec. This
threefold increase in peak systolic velocity correlates with stenosis in our
sonography laboratory.
|
|
View larger version (124K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 1E. —37-year-old man with decreasing renal function who was
referred for sonography to exclude hydronephrosis. After immunosuppression was
decreased in patient, mass became markedly smaller and renal function
improved. Coronal T1-weighted spin-echo MR image (TR/TE, 500/25) shows
intimate relationship of mass (arrow) to renal allograft and
resultant hydronephrosis. Note isointensity of T1 signal of in relation to
with renal allograft parenchyma.
|
|
View larger version (153K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2A. —49-year-old man with increased serum creatinine level 3
months after transplantation. Subsequent allograft nephrectomy histologically
confirmed mass as posttransplantation lymphoproliferative disorder.
Longitudinal sonogram shows 4.5 x 3.6 cm heterogeneous mass
(cursors) adjacent to renal allograft hilum.
|
|
View larger version (111K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2B. —49-year-old man with increased serum creatinine level 3
months after transplantation. Subsequent allograft nephrectomy histologically
confirmed mass as posttransplantation lymphoproliferative disorder. Color
Doppler sonogram shows small branching feeder vessels from main renal artery
into mass. These small vessels had arterial-type pulsatile waveform on
spectral Doppler interrogation.
|
|
View larger version (133K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 2C. —49-year-old man with increased serum creatinine level 3
months after transplantation. Subsequent allograft nephrectomy histologically
confirmed mass as posttransplantation lymphoproliferative disorder.
Contrast-enhanced CT scan shows central low attenuation within heterogeneous,
mildly enhancing mass (arrows).
|
|
View larger version (131K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3A. —37-year-old woman with doubling of serum creatinine level to
2.4 mg/dL 7 months after transplantation. Subsequent allograft nephrectomy
confirmed small pararenal mass as posttransplantation lymphoproliferative
disorder. Transverse sonogram shows small hypoechoic mass (cursors)
near renal allograft. Although unusual, increased through transmission can be
seen in solid masses. Echogenicity was not characteristic of simple
lymphocele, and at 7 months after transplantation, hematoma is unlikely.
|
|
View larger version (98K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 3B. —37-year-old woman with doubling of serum creatinine level to
2.4 mg/dL 7 months after transplantation. Subsequent allograft nephrectomy
confirmed small pararenal mass as posttransplantation lymphoproliferative
disorder. Axial fast spin-echo T2-weighted MR image (TR/TE, 5000/85) shows
well-marginated solid mass (arrow). Although some slightly higher T2
signal centrally can be seen, note mass is predominantly of lower signal
intensity than renal parenchyma.
|
|
View larger version (138K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4A. —20-year-old woman with decreased renal function 14 months
after transplantation. Allograft nephrectomy confirmed posttransplantation
lymphoproliferative disorder. Axial fast multiplanar spoiled gradient-echo
T1-weighted MR image (TR/TE, 140/4.2; flip angle, 70°) shows predominantly
low-signal mass (arrow).
|
|
View larger version (132K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 4B. —20-year-old woman with decreased renal function 14 months
after transplantation. Allograft nephrectomy confirmed posttransplantation
lymphoproliferative disorder. MR image acquired after administration of
gadolinium with same sequence as that in A shows slight enhancement,
predominantly in periphery (arrow).
|
|
View larger version (148K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 5A. —50-year-old woman with fever and decreasing renal function 6
months after transplantation. Allograft nephrectomy confirmed
posttransplantation lymphoproliferative disorder. Longitudinal sonogram shows
5 x 4 cm complex mass (cursors) slightly separate from renal
allograft hilum (arrow).
|
|
View larger version (126K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 5B. —50-year-old woman with fever and decreasing renal function 6
months after transplantation. Allograft nephrectomy confirmed
posttransplantation lymphoproliferative disorder. Longitudinal color Doppler
sonogram shows mass encircling main and accessory renal artery as they arise
from external iliac artery (IL). M = mass.
|
|
View larger version (127K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 5C. —50-year-old woman with fever and decreasing renal function 6
months after transplantation. Allograft nephrectomy confirmed
posttransplantation lymphoproliferative disorder. Unenhanced CT scan shows
mass (arrow) adjacent to inferior aspect of allograft. Note metallic
streak artifacts from vascular anastomosis surgical clips.
|
|
View larger version (151K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 6A. —45-year-old woman with history of episode of rejection
presenting with decreasing renal function. Allograft nephrectomy confirmed
posttransplantation lymphoproliferative disorder. Longitudinal sonogram shows
heterogeneous hilar mass (cursors). Note hydronephrosis.
|
|
View larger version (111K):
[in this window]
[in a new window]
[as a PowerPoint slide]
|
Fig. 6B. —45-year-old woman with history of episode of rejection
presenting with decreasing renal function. Allograft nephrectomy confirmed
posttransplantation lymphoproliferative disorder. Percutaneous nephrostogram
shows mass effect on ureter (arrow) with medial displacement and mild
narrowing.
|
|
Hydronephrosis was observed in five patients. The mass was always located
in close proximity to the transplant renal artery and vein, appearing to
circumferentially surround the hilar vessels. Feeder vessels from the main
renal artery into the mass could occasionally be seen with color Doppler
sonography (Fig.
2A,2B,2C).
In eight patients, apparent focal stenosis of the renal vessels due to mass
effect (the main renal artery, 4 patients; the main renal vein, 3 patients;
both artery and vein, 1 patient) was suspected with spectral Doppler
interrogation. Stenosis was suspected when blood flow maximum velocity shift
within the renal vessels was greater than twice that of the adjacent upstream
iliac vessels (Fig.
1A,1B,1C,1D,1E).
CT
Nine patients underwent CT of the abdomen and pelvis. Because of worsening
renal function, six of these examinations were performed without IV contrast
material. All unenhanced studies showed a soft-tissue mass adjacent to the
renal transplant hilum. When IV contrast material was administered, the hilar
mass showed mild enhancement (Fig.
2A,2B,2C).
With the one exception previously noted, no other patients in our series had
enlarged pelvic or abdominal lymph nodes or other organs involved.
MR Imaging
Six patients underwent MR imaging of the pelvis. Images obtained in the
axial and coronal planes clearly showed the hilar mass. The signal
characteristics of the hilar mass were usually isointense on T1-weighted and
slightly decreased on T2-weighted images with respect to the renal allograft
parenchyma (Figs.
1A,1B,1C,1D,1E,
3A,3B,
and
4A,4B).
Mild and mostly peripheral contrast enhancement with gadolinium was
present.
Discussion
An increased frequency of posttransplantation lymphoproliferative disorder
localized to the renal allograft has been attributed to the increased use of
antilymphocyte antibodies (e.g., OKT3 [anti-CD3 monoclonal antibody]) for
immunosuppression [2].
Microscopic involvement localized to the renal allograft was the most common
manifestation of posttransplantation lymphoproliferative disorder in a
retrospective review of a renal transplantation population
[4]. Other reports have
described macroscopic involvement limited to the allograft with a mass
adjacent to the renal hilum
[5,6,7,8,
10]. Our experience confirms
that posttransplantation lymphoproliferative disorder localized to the
allograft is a common manifestation with a renal hilar mass as an initial
imaging finding.
All our patients presented with worsening renal function. Sonography of the
renal allograft is a common request in this clinical scenario. All sonograms
depicted the hilar mass well enough for the radiologist to include
posttransplantation lymphoproliferative disorder in the differential diagnosis
of a sonographically complex mass in this setting (including nonneoplastic
causes such as abscess, resolving hematoma, seroma, and complicated
lymphocele). We noted hydronephrosis in five of the 12 patients. Sonography
has also been sufficient to monitor the decreasing size of the hilar mass in
the patients who responded to decreased maintenance immunosuppression.
CT is helpful to evaluate whether the disease is limited to the renal hilum
or is associated with intraabdominal or pelvic adenopathy. Because one patient
in our series with retroperitoneal adenopathy had a progressively fulminant
course, this finding may suggest a worse clinical outcome. Because of the
tenuous renal function of some patients, an unenhanced study may be
preferable, but it renders the relationship of the renal hilar mass to the
transplant harder to depict. In this setting, MR imaging, with its multiplanar
views, can be a useful adjunct in diagnosis.
In 1999, Ali et al. [8]
described the MR imaging appearance of five patients with posttransplantation
lymphoproliferative disorder localized in the renal hilum. As in our series,
these investigators noted the predilection of posttransplantation
lymphoproliferative disorder for involvement of the renal hilum and the
typical MR imaging pattern of hypointensity with regard to renal parenchyma on
T2-weighted images and minimal enhancement after gadolinium administration.
This pattern differs from that of the other diagnostic entities mentioned
previously and may further increase confidence in the imaging diagnosis of
posttransplantation lymphoproliferative disorder. An accurate noninvasive
method to suggest this diagnosis is helpful because renal vessel encasement by
the mass increases the risk of percutaneous biopsy and because the cytologic
diagnosis of posttransplantation lymphoproliferative disorder using
fine-needle aspiration can be difficult
[8].
Some of the Doppler sonographic examinations suggested an apparent focal
stenosis of the renal vessels surrounded by these masses when it appeared
there was a significant focal increase in peak systolic velocity. Inaccuracies
in Doppler measurements are possible, especially if the entire renal artery
cannot be visualized or the angle of Doppler interrogation is greater than
60°. Although renal vascular stenosis in a cadaveric allograft with a
Carrell aortic patch is occasionally caused by anastomotic narrowing, our
experience stresses the need to exclude an adjacent hilar mass, especially if
dilation of the urinary collecting system is also observed. Visualization of
the entire renal artery and vein is necessary to exclude a focal mass because
it may not be seen on standard views focused on the transplant kidney. Because
of renal dysfunction, correlative angiographic studies were not performed.
Recent advances in the development of sonographic contrast agents and
gadolinium-enhanced MR angiography may be useful in the future to further
evaluate possible renal vascular stenosis.
This series of 12 patients confirms and expands the recent description of
the predilection of posttransplantation lymphoproliferative disorder to encase
the renal allograft hilar structures as well as its MR imaging pattern. The
lack of other adenopathy or any mass within the renal parenchyma was common in
our patients. In our experience, sonography is effective in showing this focal
manifestation for the diagnosis of posttransplantation disorder. CT or MR
imaging may be useful in excluding other abdominal adenopathy. The MR image
signal intensity pattern of posttransplantation lymphoproliferative disorder
can increase diagnostic confidence. This localized form of posttransplantation
lymphoproliferative disorder should be considered as a diagnostic possibility
when a complex solid renal hilar mass is noted, especially during the first
year after transplantation.
References
-
Hanto DW, Gajl-Peczlaska KJ, Frizzera G, et al. Epstein-Barr virus
(EBV) induced polyclonal and monoclonal B-cell lymphoproliferative diseases
occurring after renal transplantation. Ann Surg
1983;198:365
-369
-
Cockfield SM, Prieksaitis JK, Jewell LD, Parfrey NA.
Post-transplant lymphoproliferative disorder in renal allograft recipients.
Transplantation
1993;56:88
-96[Medline]
-
Dodd GD III, Greenler DP, Confer SR. Thoracic and abdominal
manifestations of lymphoma occurring in the immunocompromised patient.
Radiol Clin North Am
1992;30:597
-610[Medline]
-
Miller WT Jr, Siegel SG, Montone KT. Posttransplantation
lymphoproliferative disorder: changing manifestations of disease in a renal
transplant population. Crit Rev Diagn Imaging
1997;36:569
-585
-
Olcott EW, Goldstein RB, Salvatierra O. Lymphoma presenting as
allograft hematoma in a renal transplant recipient. J Ultrasound
Med 1990;9:239
-241[Medline]
-
Goral S, Felgar R, Shappell S. Posttransplantation
lymphoproliferative disorder in a renal allograft recipient. Am J
Kidney Dis 1997;30:301
-307[Medline]
-
Palmer BF, Sagalowsky AI, McQuitty DA, Dawidson I, Vazquez MA, Lu
CY. Lymphoproliferative disease presenting as obstructive uropathy after renal
transplantation. J Urol
1995;153:392
-394[Medline]
-
Ali MG, Coakley FV, Hricak H, Bretan PN. Complex
posttransplantation abnormalities of renal allografts: evaluation with MR
imaging. Radiology
1999;211:95
-100[Abstract/Free Full Text]
-
Kew CE, Lopez-Ben R, Smith JK, et al. Posttransplant
lymphoproliferative disorder localized near the allograft in renal
transplantation. Transplantation
2000;69:809
-814[Medline]
-
Squiers EC, West JC, Leonard D, et al. Epstein-Barr
virus-associated posttransplant lymphoproliferative disorder presenting as
perirenal transplant lymphocele. Transplantation
1993;56:1278
-1279[Medline]
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati What's this?
This article has been cited by other articles:
|
|
|
|
 
C. Sebastia, S. Quiroga, R. Boye, C. Cantarell, M. Fernandez-Planas, and A. Alvarez
Helical CT in Renal Transplantation: Normal Findings and Early and Late Complications
RadioGraphics,
September 1, 2001;
21(5):
1103 - 1117.
[Abstract]
[Full Text]
[PDF]
|
|
|
Top
Abstract
Introduction
