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 Previous Article | Table of Contents | Next Article 
Blood, Vol. 94 No. 2 (July 15), 1999:
pp. 429-433
Whole-Body Positron Emission Tomography Using
18F-Fluorodeoxyglucose for Posttreatment Evaluation in
Hodgkin's Disease and Non-Hodgkin's Lymphoma Has Higher Diagnostic
and Prognostic Value Than Classical Computed Tomography Scan Imaging
By
G. Jerusalem,
Y. Beguin,
M.F. Fassotte,
F. Najjar,
P. Paulus,
P. Rigo, and
G. Fillet
From the Department of Medicine, Divisions of Oncology-Hematology and
Nuclear Medicine, University of Liège, Liège, Belgium.
 |
ABSTRACT |
A residual mass after treatment of lymphoma is a clinical challenge,
because it may represent vital tumor as well as tissue fibrosis.
Metabolic imaging by 18F-fluorodeoxyglucose
(18F-FDG) positron emission tomography (PET)
offers the advantage of functional tissue characterization that is
largely independent of morphologic criteria. We compared
18F-FDG PET to computed tomography (CT) in the
posttreatment evaluation of 54 patients with Hodgkin's disease (HD) or
intermediate/high-grade non-Hodgkin's lymphoma (NHL). Residual masses
on CT were observed in 13 of 19 patients with HD and 11 of 35 patients
with NHL. Five of 24 patients with residual masses on CT versus 1 of 30 patients without residual masses presented a positive
18F-FDG PET study. Relapse occurred in all 6 patients
(100%) with a positive 18F-FDG PET, 5 of 19 patients
(26%) with residual masses on CT but negative 18F-FDG PET,
and 3 of 29 patients (10%) with negative CT scan and 18F-FDG PET studies (P  .0001). We
observed a higher relapse and death rate in patients with residual
masses at CT compared with patients without residual masses at CT
(progression-free survival at 1 year: 62 ± 10 v
88 ± 7%, P = .0045; overall survival at 1 year: 77 ± 5 v 95 ± 5%, P = .0038). A positive
18F-FDG PET study was even more consistently associated
with poorer survival: compared with patients with a negative
18F-FDG PET study, the 1-year progression-free survival was
0% versus 86% ± 5% (P < .0001) and the 1-year
overall survival was 50% ± 20% versus 92% ± 4% (P < .0001). The detection of vital tumor by 18F-FDG PET after
the end of treatment has a higher predictive value for relapse than
classical CT scan imaging (positive predictive value: 100% v
42%). This could help identify patients requiring intensification
immediately after completion of chemotherapy. However,
18F-FDG PET mainly predicts for early progression but
cannot exclude the presence of minimal residual disease, possibly
leading to a later relapse.
© 1999 by The American Society of Hematology.
| |
INTRODUCTION |
ONE OF THE MOST challenging aspects in
the imaging of lymphomas is the assessment of response to treatment.
Differentiation of tumor from fibrosis within residual radiographic
masses represents a problem of interpretation for both Hodgkin's
disease (HD) and non-Hodgkin's lymphoma (NHL). Although up to 64% of
lymphoma patients may present a residual mass after completion of
therapy, only 18% of these patients will eventually
relapse.1,2 In patients with demonstration of persisting
viable tumor, it could be reasonable to use salvage therapy and
possibly hematopoietic stem cell transplantation at the time of minimal
disease rather than at the time of clinically overt relapse. There are
no reliable radiographic characteristics that permit differentiation
between malignant and fibrotic or necrotic tissue. Positron emission
tomography (PET) scan with the glucose analogue
2-(F-18)-fluoro-2-deoxy-D-glucose (18F-FDG) has emerged as
a clinical method for staging and monitoring responses to treatment in
a variety of cancers.3 Increased glycolysis is one of the
most distinctive biochemical features of malignant cells, resulting
from amplification of the glucose transporter protein at the tumor cell
surface as well as from increased activity of hexokinase.4
Like glucose, 18F-FDG is transported into cells by a
glucose transporter protein and rapidly converted into
18F-FDG-6-phosphate. Because the latter is not a substrate
for glucose-6-phosphate isomerase, it is biochemically trapped in
metabolising tissues.5 In the present study, we evaluated
the role of 18F-FDG PET compared with computed tomography
(CT) in the posttreatment evaluation of patients with HD and aggressive NHL.
| |
PATIENTS AND METHODS |
Patients.
Fifty-four patients were included in our study. They were recruited
prospectively between June 1994 and February 1998. Patients with
clinically progressive disease under chemotherapy were excluded. Nineteen had HD and 35 had intermediate-grade or high-grade NHL (Working Formulation groups D through J). Patient characteristics are listed in Table 1. All patients gave
fully informed oral consent for the study.
Baseline evaluation.
Routine staging methods at diagnosis included at least clinical
examination, laboratory screening, chest x-ray, CT of chest and
abdomen, and bone marrow biopsy. Most patients (40/54) were also
evaluated by 18F-FDG PET at diagnosis.
End of treatment evaluation.
One to 3 months after completion of therapy, all patients were
re-evaluated by whole body 18F-FDG PET and by CT.
Intravenous contrast enhancement was used in every CT examination and
all sites previously involved by lymphoma were reanalyzed.
Posttreatment 18F-FDG PET scans were first interpreted
without knowledge about clinical, CT, or previous PET data. In the case of abnormal 18F-FDG uptake, we then correlated our findings
with clinical information and CT studies. Indeed, strong
18F-FDG uptake is not only observed in malignant neoplastic
tissue, but also can be seen in inflammatory lesions (sarcoidosis,
tuberculosis, fungal infections, abdominal abscesses, etc). We thus
considered that the abnormal 18F-FDG uptake was related to
residual tumor, except when the clinical data clearly indicated uptake
in nonmalignant lesions. We finally compared posttreatment PET data
with pretreatment studies in the 40 patients in whom such studies were available.
18F-FDG PET studies.
Whole-body PET using 18F-FDG was performed with a Penn Pet
240-H Scanner (UGM, Philadelphia, PA). Six to eight millicuries of 18F-FDG was administered intravenously, and emission scans
were recorded 45 to 90 minutes later. All patients were asked to fast for at least 6 hours before the study. A whole-body acquisition was
performed from the cervical to the inguinal regions. It consisted of 10 to 12 separate overlapping acquisitions each covering 12.8 cm and
performed during 4 minutes. Each subsequent acquisition was performed
after a 6.4-cm displacement of the table. The total time of image
acquisition was approximately 50 minutes. Images were reconstructed
using filtered back projection with a Hanning filter and
were reoriented in transverse, coronal, and sagittal planes. A 4-mm
voxel size was used. Isotropic 3D resolution was better than 8 mm. PET
interpretation was performed in a qualitative manner without
attenuation correction. All PET images were reviewed by one
investigator (G.J.). Any focus of increased 18F-FDG uptake
over background not located in areas of normal 18F-FDG
uptake (central nervous system, heart, digestive tract, thyroid, and
muscles) and/or excretion (urinary tract) was considered positive for
tumor. Furosemide (20 mg in slow intravenous [IV] injection) was
administered in patients with suspected pelvic abnormalities to enhance
18F-FDG urinary elimination. These patients were studied
later (60 to 90 minutes) and after voiding. Diazepam (5 mg) was
administered orally before 18F-FDG administration in some
tense patients to prevent muscular uptake.
Statistical methods.
Comparison of groups for the probability of relapse was performed with
Fisher's exact tests or chi-square tests with Yates' correction as
appropriate. Overall survival (OS) and progression-free survival (PFS)
were calculated by Kaplan-Meier survival analysis, and comparison
between groups was performed by the log-rank test.
| |
RESULTS |
Posttreatment evaluation: Residual masses at CT.
According to routine CT staging and clinical examination, 30 patients
achieved a complete remission (CR), whereas residual masses were found
in 24 patients (Table 2). Thoracic masses
were observed in 12 patients, abdominal masses in 6 patients,
peripheral masses in 4 patients, and thoracic plus abdominal masses in
2 patients. The greatest diameter of residual masses was greater than 1 to 3 cm in 16 patients, 3.5 to 5 cm in 3 patients, 5.5 to 10 cm in 3 patients, and greater than 10 cm in 2 patients. The incidence of
residual masses was higher in patients with HD compared with those with
NHL (13/19 [68%] v 11/35 [31%], P = .0116). 18F-FDG PET was positive in 5 patients with residual
masses: 1 of 13 patients with HD and 4 of 11 patients with NHL (not
significant [NS]). Therefore, although more patients
with HD presented residual masses at the end of therapy, increased
metabolic activity in residual masses was more frequent in NHL
patients. The greatest diameter of residual masses at CT was greater
than 1 to 3 cm in all 5 patients with positive 18F-FDG PET.
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Table 2.
Outcome According to the Results of Posttreatment CT
Scan and 18F-FDG PET Studies in 54 Patients With HD or
NHL
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Posttreatment evaluation: CT scan versus 18F-FDG PET.
Results of posttreatment 18F-FDG PET and CT scan
evaluations are presented in Table 2, and examples of positive and
negative 18F-FDG PET studies are shown in
Figs 1 and 2.
Seven of 54 patients, 5 with and 2 without residual masses, presented a
positive 18F-FDG PET study. In 1 patient, clinical data
clearly indicated that 18F-FDG uptake had nothing to do
with tumor. It was localized exclusively at the cutaneous site of a
recent excision of a benign lesion. The other 6 showed
18F-FDG uptake in areas previously involved by lymphoma.
Correlation with pretreatment PET never changed the interpretation of
residual abnormal 18F-FDG uptake in posttreatment studies.
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| Fig 1.
18F-FDG PET before and after treatment in a
patient with high-grade NHL relapsing 1 month after the
18F-FDG PET study. On the left, 18F-FDG PET
before treatment: multiple lymph node (cervical, axillary, mediastinal,
hilar, iliac, and retroperitoneal) and splenic infiltration. On the
right, 18F-FDG PET after treatment: residual
18F-FDG uptake in hilar, retroperitoneal lymph nodes, and
spleen. The CT scan indicated residual masses in the same areas as
18F-FDG PET.
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| Fig 2.
CT and 18F-FDG PET studies at the end of
treatment in a case of relapsed HD remaining in clinical CR after a
follow-up of 42 months. (A) The CT study at the end of treatment showed
a large residual mediastinal mass. (B) The 18F-FDG PET
study of this patient was negative.
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The 5 patients with residual masses on CT progressed rapidly after
evaluation at sites with abnormal 18F-FDG uptake. The only
patient with a positive 18F-FDG PET study but no residual
mass relapsed 9 months after completion of therapy. Among the 19 patients with residual masses but negative 18F-FDG PET
studies, 14 remained in clinical remission after a median of 21 months,
whereas 5 patients progressed rapidly. Four of them relapsed outside
the residual masses. Among the 29 patients with no residual mass and
negative 18F-FDG PET study, 26 remained in CR after a
median of 23 months, whereas 3 patients relapsed at a median of 12 months. Thus, the detection of vital tumor by 18F-FDG PET
after the end of treatment had a higher predictive value for relapse
than classical CT scan imaging. Whereas only 5 of 19 patients with
residual masses but negative 18F-FDG PET relapsed, all 5 patients with 18F-FDG uptake in residual masses progressed
(P = .0137). Positivity of 18F-FDG PET was
associated with poorer outcome (6/6 relapses) compared with negative
18F-FDG PET (8/48 relapses; P < .0001).
Kaplan-Meier analysis of PFS (0% v 86% ± 5% at 1 year,
P < .0001; Fig 3) and OS (50% ± 20% v 92% ± 4% at 1 year, P < .0001)
were thus significantly different among these two groups. On the other
hand, the presence of residual masses was less consistently associated
with poorer outcome than the positivity of 18F-FDG PET: 10 of 24 relapses in the presence of a mass compared with 4 of 30 relapses
in the absence of a residual mass (P = .0284). Kaplan-Meier
analysis of PFS (62% ± 10% v 88% ± 7% at
1 year, P = .0045; Fig 4) and OS
(77% ± 5% v 95% ± 5% at 1 year, P = .0038) were also significantly different among these two groups. Combining the
results of CT and PET permitted to define three prognostic groups
(Fig 5; P < .0001). The good-risk
patients (n = 29) had negative CT and PET, with a PFS of 87% and an OS
of 95% at 2 years. The intermediate-risk group (n = 19) had residual
masses but a negative PET. Their PFS (60% at 2 years, P = .0551) and OS (70% at 2 years, P = .0470) were lower. The
high-risk patients (n = 6) had a positive PET with strikingly reduced
PFS (P < .0001) and OS (P < .0001). The positive
predictive value (defined as true positive for relapse and/or positive
biopsy) was 100% (6/6 patients) for 18F-FDG PET but only
42% (10/24 patients) for residual masses (P = .0354). The
negative predictive value (defined as true negative by persistent
clinical CR) was 83% (40/48 patients) for 18F-FDG PET and
87% (26/30 patients) for residual masses (NS).
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| Fig 3.
Kaplan-Meier estimate of PFS in 6 patients with positive
18F-FDG PET compared with 48 patients with negative
18F-FDG PET (P < .0001).
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| Fig 4.
Kaplan-Meier estimate of PFS in 24 patients with residual
masses on CT compared with 30 patients without residual masses on CT
(P = .0045).
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| Fig 5.
Kaplan-Meier estimate of PFS in 29 patients with negative
PET and CT scans compared with 19 patients with positive CT but
negative PET and 6 patients with positive PET (P < .0001).
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| |
DISCUSSION |
The introduction of high-resolution CT and magnetic resonance imaging
(MRI) has improved the ability to identify morphological alterations by
radiological methods. However, there are no reliable radiographic
characteristics for CT that permit differentiation between malignant
and fibrotic or necrotic tissue. MRI can potentially discriminate
fibrosis from lymphoma, because different signal characteristics have
been reported for malignant tissue, normal tissue, and fibrosis. On
T2-weighted images, active tumor is associated with high
signal intensity, whereas fibrosis is characterized by low signal
intensity.6-8 Hill et al9 reported that MRI provided clinically useful prognostic information. Thirty-four patients
treated for HD or intermediate/high-grade NHL were included in their
prospective study. The good specificity (90%) but low sensitivity
(45%) demonstrated that MRI was not an ideal investigation. Devizzi et
al10 used MRI to study 47 patients with mediastinal HD at
the end of treatment. They reported 2 true-positive, 4 false-positive, 1 false-negative, and 40 true-negative MRI studies. Restaging by
chest-abdominal CT and 67Ga scintigraphy was also
performed. Results of all three tests were correlated with disease
outcome during follow-up, and a cost/benefit ratio for each test was
determined. The investigators concluded that 67Ga
scintigraphy proved as accurate as MRI in confirming mediastinal CR,
whereas the specificity of CT was much lower. Considering the higher
cost of MRI, this study should only be performed in patients with an
initial negative 67Ga scan at diagnosis presenting a
residual mediastinal mass by CT.
Other studies comparing 67Ga scintigraphy and MRI indicate
similar sensitivity and specificity for assessing tumor activity in
residual masses.11-13 67Ga scintigraphy has
thus become a standard procedure for the posttreatment evaluation of
patients with lymphoma.1,14 Iosilevsky et al15 have shown in an animal model that tumor uptake of 67Ga
after radiation and chemotherapy closely paralleled the number of
residual neoplastic cells. However, 67Ga scintigraphy
should always be performed before treatment to determine if the
individual patient has a gallium-avid lymphoma.16 The
sensitivity for staging of lymphoma varies with the localization of the
lesion: 96% for a chest lesion, 60% for an abdominal lesion, and 83%
for a peripheral lesion.1,17 Attention to technical details
and correlation with the results of CT scans is mandatory, because even
low abnormal 67Ga uptake should be considered as an
indicator of residual tumor.18 In patients younger than 25 years of age, an enlarged mass in the anterior mediastinum during the 6 months after completion of treatment can indicate a regenerating
thymus19 and the thymus can take up gallium.20
Unfortunately, false-positive thymus uptake was also reported for
18F-FDG PET in this patient population within this time
frame.21
Despite the important role of 67Ga scintigraphy in lymphoma
imaging, it appears that 18F-FDG PET may be a more
effective method. 18F-FDG PET scanning is likely to be
favored by clinicians and patients alike because of same day imaging
and the inherent superiority of PET imaging methods over standard gamma
camera imaging in terms of sensitivity and resolution. Residual as well
as recurrent malignant lymphoma could be accurately diagnosed by
18F-FDG PET.22 De Wit et al23
reported a high predictive value of 18F-FDG PET performed
for evaluation of residual masses after treatment of lymphoma. Residual
masses were found in 32 of 34 patients using routine methods.
18F-FDG PET was negative in 17 patients and none of them
relapsed (median follow-up, 14 months). 18F-FDG PET was
positive in 17 patients and 8 patients relapsed. Unfortunately, 4 patients received radiotherapy after PET and did not get another PET
after radiotherapy. So, the final 18F-FDG PET uptake after
completed therapy is not known (no relapse after an average follow-up
of 13 months). There were at least 3 false-positive results inside and
2 false-positive results outside residual masses. There was a trend for
18F-FDG PET to be more sensitive as well as more specific
than CT. However, the main disadvantage of this study was the short
follow-up. The investigators concluded that 18F-FDG PET is
the most helpful noninvasive modality in differentiating recurrence or
residual disease from fibrosis.
Our data indicate that whole-body 18F-FDG PET has higher
diagnostic and prognostic value than classical CT scan imaging for posttreatment evaluation in HD as well as in NHL. We report an excellent positive predictive value (100%) for 18F-FDG
PET-positive studies. In fact, the false-positive result outside
residual masses (as reported by De Wit23)
could be promptly interpreted with available clinical information. The
positive predictive value is largely in favor of 18F-FDG
PET compared with computed tomography (6 of 6 patients [100%] v 10 of 24 patients [42%]). These relapses occurred rapidly
after posttreatment evaluation. The negative predictive value was 83% for 18F-FDG PET (40/48 patients remained in clinical CR)
and 87% for residual masses (26/30 patients remained in clinical CR).
A negative 18F-FDG PET thus cannot exclude the presence of
minimal residual disease possibly leading to a later relapse. Clinical
relapse in 18F-FDG PET negative patients was observed more
frequently in those with (5 of 19 patients) than those without (3 of 29 patients) residual masses. Interestingly, 4 of the 5 relapses in
patients with residual masses occurred outside of these masses.
Residual masses in 18F-FDG PET-negative patients thus
indicate a higher risk of relapse but rarely predict the site of relapse.
Our study definitively indicates the value of adding PET to CT for the
noninvasive evaluation of residual masses. Pretreatment 18F-FDG PET is useful only if complete clinical and CT data
are not available. Posttreatment PET studies are useful to localize abnormal 18F-FDG uptake inside or outside of known residual
masses at CT. If 18F-FDG uptake is outside of residual
masses, inflammatory lesions have first to be excluded. If
18F-FDG uptake is inside residual masses, strong
consideration should be given to additional therapy. In routine
clinical circumstances one would combine the results of PET with CT and
clinical information.
Further studies are warranted that compare 18F-FDG PET to
67Ga scintigraphy and MRI studies to determine the best
cost-benefit approach of patients with residual masses at the end of
treatment. Other studies will determine if posttreatment evaluation
based only on 18F-FDG PET studies is a valid alternative to
conventional radiological examination.
| |
FOOTNOTES |
Submitted November 17, 1998; accepted March 9, 1999.
Y.B. is senior research associate of the National Fund for Scientific
Research, Belgium.
The publication costs of this
article were defrayed in part by
page charge payment. This article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. section
1734 solely to indicate this fact.
Address reprint requests to G. Jerusalem, MD, Oncology-Hematology, CHU
Sart Tilman, B35, B-4000-Liege 1, Belgium.
| |
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JAMA,
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P. Seam, M. E. Juweid, and B. D. Cheson
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[Abstract]
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[Abstract]
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C. Lin, E. Itti, C. Haioun, Y. Petegnief, A. Luciani, J. Dupuis, G. Paone, J.-N. Talbot, A. Rahmouni, and M. Meignan
Early 18F-FDG PET for Prediction of Prognosis in Patients with Diffuse Large B-Cell Lymphoma: SUV-Based Assessment Versus Visual Analysis
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R. Advani, L. Maeda, P. Lavori, A. Quon, R. Hoppe, S. Breslin, S. A. Rosenberg, and S. J. Horning
Impact of Positive Positron Emission Tomography on Prediction of Freedom From Progression After Stanford V Chemotherapy in Hodgkin's Disease
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[Abstract]
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N. G. Schaefer, C. Taverna, K. Strobel, C. Wastl, M. Kurrer, and T. F. Hany
Hodgkin Disease: Diagnostic Value of FDG PET/CT after First-Line Therapy--Is Biopsy of FDG-avid Lesions Still Needed?
Radiology,
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[Abstract]
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K. Herrmann, H. A. Wieder, A. K. Buck, M. Schoffel, B.-J. Krause, F. Fend, T. Schuster, C. Meyer zum Buschenfelde, H.-J. Wester, J. Duyster, et al.
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TOP
ABSTRACT
INTRODUCTION