Original article

Early therapy monitoring with FDG-PET in aggressive

non-Hodgkin’s lymphoma and Hodgkin’s lymphoma
Tatsuo Torizuka1, Fumitoshi Nakamura1, Toshihiko Kanno1, Masami Futatsubashi2, Etsuji Yoshikawa2,
Hiroyuki Okada2, Masahide Kobayashi3, Yasuomi Ouchi1
1 PositronMedical Center, Hamamatsu Medical Center, Hamakita, Shizuoka, Japan
2 CentralResearch Laboratory, Hamamatsu Photonics K.K., Hamakita, Japan
3 Department of Hematology, Hamamatsu Medical Center, Hamamatsu, Japan

Received: 22 May 2003 / Accepted: 18 August 2003 / Published online: 22 October 2003
© Springer-Verlag 2003

Abstract. This study was designed to determine the
value of 2-[fluorine-18]-fluoro-2-deoxy-D-glucose posi-
tron emission tomography (FDG-PET) in the early as-
sessment of therapy response in lymphoma patients. We
studied 20 patients with pathologically proven lympho-
ma, including 17 patients with aggressive non-Hodgkin’s
lymphoma and three patients with Hodgkin’s lymphoma.
All patients underwent whole-body FDG-PET imaging at
baseline and after 1–2 cycles of chemotherapy. PET im-
ages were analysed visually and quantitatively by calcu-
lating the standardised uptake value (SUV). In each pa-
tient, we measured the SUV of the tumour demonstrating
the highest FDG uptake at baseline study and the SUV of
the same tumour after 1–2 cycles of therapy. The achieve-
ment of complete response was assessed on the basis of a
combination of clinical findings and the results of con-
ventional imaging modalities. Follow-up of progression-
free survival (PFS) was obtained for the validation of
PET data. Of the 20 patients, ten achieved complete re-
mission at the completion of chemotherapy and the other
ten did not respond to chemotherapy. Of the ten respond-
ers, four are still in remission (PFS 24–34 months) while
the other six have relapsed (PFS 8–16 months). For the
prediction of 24-month clinical outcome, visual analysis
of PET after 1–2 cycles showed high sensitivity (87.5%)
and accuracy (80%) but low specificity (50%). Compari-
son with the baseline SUVs revealed that the responders
showed a significantly greater percent reduction in SUV
after 1–2 cycles of therapy as compared with the non-
responders (81.2%±9.5% vs 35.0%±20.2%, P<0.001). In
addition, using 60% reduction as a cut-off value, the re-
sponders were clearly separated from the non-responders,
with the exception of one non-responder. In conclusion,
when performed early during chemotherapy, FDG-PET
Tatsuo Torizuka (✉)
Positron Medical Center, Hamamatsu Medical Center,
5000 Hirakuchi, 434-0041 Hamakita, Shizuoka, Japan
e-mail: tatsuo@pmc.hmedc.or.jp
Tel.: +81-53-5850366, Fax: +81-53-5850367
may be predictive of clinical outcome and allows differ-
entiation of responders from non-responders in cases of
aggressive lymphoma.
Keywords: Aggressive malignant lymphoma – FDG-
PET – Therapy monitoring – Prognosis
Eur J Nucl Med Mol Imaging (2004) 31:22–28
DOI 10.1007/s00259-003-1333-8
Introduction
Despite advances in the treatment of aggressive non-
Hodgkin’s lymphoma (NHL) and Hodgkin’s lymphoma
(HL), only some patients respond by achieving a pro-
longed disease-free survival and cure [1, 2]. Accurate
evaluation of response to therapy is crucial in the man-
agement of patients with lymphoma, and early prediction
of therapy response could potentially identify those pa-
tients who will benefit most from standard conventional
therapy and those for whom alternative treatment strate-
gies might prove more effective. A combination of risk
factors evaluated before treatment has been shown to
predict outcome in a large cohort of patients. While the
International Prognostic Index (IPI) offers a means of
allocating patients to different prognostic groups [3], it is
based on pre-treatment prognostic factors, thereby omit-
ting response to therapy, the most significant determinant
of outcome.
X-ray computed tomography (CT) is currently the
most widely used method for initial staging and subse-
quent remission assessment. However, it is an anatomi-
cal imaging modality that relies predominantly on size
criteria for the diagnosis of lymphadenopathy and is thus
limited by its inability to detect small-volume residual
disease in normal-sized nodes. In addition, CT cannot
readily differentiate between viable disease and fibrous
tissue in residual mass during or after treatment [4]. Met-

European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 1, January 2004

abolic imaging with gallium-67 (67Ga) has been shown
to be a useful technique for remission assessment and
evaluation of residual masses following treatment of
lymphoma patients [5, 6]. Recently, 67Ga scan including
single-photon emission tomography has been reported to
be an independent predictor of outcome after 1–2 cycles
of chemotherapy [7, 8]. However, 67Ga scan is less effi-
cacious for the evaluation of deeply located small le-
sions, especially those in the abdomen or pelvis, because
of its poor resolution and physiological bowel uptake.
Over recent years, positron emission tomography
(PET) using 2-[fluorine-18]-fluoro-2-deoxy-D-glucose
(FDG) has emerged as an extremely useful technique in
clinical oncology [9, 10, 11]. Particularly since the intro-
duction of whole-body scanning, clinical applications of
FDG-PET for tumour staging and monitoring after treat-
ment have been increasing [12, 13, 14]. In contrast to the
conventional imaging methods, PET can yield metabolic
information with high-resolution images. Previous re-
ports have revealed the effectiveness of post-treatment
FDG-PET for the prediction of long-term outcome in
lymphoma patients [15, 16]. More recently, Kostakoglu
et al. reported that FDG-PET performed after one cycle
of chemotherapy had a higher prognostic value than
FDG-PET performed after the last cycle, i.e. post treat-
ment [17]. In their study, however, a dual-head coinci-
dence gamma camera was used, instead of a dedicated
full-ring PET scanner. It is known that dual-head coinci-
dence gamma cameras have inferior sensitivity for tu-
mour detection as compared to dedicated PET scanners
[18, 19]. This study was designed to evaluate the predic-
tive value for clinical outcome of FDG-PET when per-
formed early during chemotherapy in patients with ag-
gressive NHL or HL, using a dedicated PET scanner.
Materials and methods
Patients. Whole-body FDG-PET studies were performed on 20
patients with histologically proven aggressive NHL or HL (age
range, 29–72 years; mean age, 55 years). Lymphoma was classi-
fied histologically according to the World Health Organisation
Classification. NHL was diagnosed in 17 patients, including ten
with diffuse large B-cell lymphoma, four with angioimmunoblas-
tic T-cell lymphoma, two with peripheral T-cell lymphoma and
one with adult T-cell lymphoma; HL was diagnosed in three pa-
tients. Seventeen patients (14 NHL, 3 HL) were studied at initial
staging before treatment and three with NHL were studied at re-
lapse before salvage chemotherapy. Of these 17 patients, two had
stage II, eight had stage III and seven had stage IV at initial stag-
ing. All three HL patients had B symptoms. Patients were treated
with the following chemotherapeutic combinations: 12 patients
with NHL received the CHOP regimen (cyclophosphamide, doxo-
rubicin, vincristine and prednisone), three patients with HL re-
ceived the COPP-ABV regimen (cyclophosphamide, vincristine,
procarbazine, prednisone, doxorubicin, bleomycin and vinblas-
tine) and the other five patients, including the three relapsing pa-
tients, received other chemotherapeutic combinations. All patients
provided written informed consent for participation in the study.
European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 1, January 2004
23
PET imaging All 20 patients underwent FDG-PET studies before
therapy and after one (n=6) or two (n=14) cycles of chemotherapy.
We used the whole-body PET scanner SHR22000 (Hamamatsu
Photonics, K.K., Hamamatsu, Japan) [14]. The SHR22000 scanner
permits simultaneous acquisition of 63 transverse planes of
3.6-mm thickness encompassing a 23.0-cm axial field of view. All
patients fasted for at least 5 h before PET studies. Serum glucose
levels measured at the time of FDG injection were normal in all
patients. Whole-body emission scans were performed 60 min after
intravenous administration of FDG (400–500 MBq) [20]. Trans-
mission scans for segmented attenuation correction were then ac-
quired with a germanium-68 external ring source. To minimise the
accumulation of FDG activity in the urinary bladder, patients were
asked to void just before the start of the emission scan. Transaxial,
coronal and sagittal images were reconstructed by means of the
ordered subsets-expectation maximisation method. The average
reconstructed x-y spatial resolution was about 4.0-mm full-width
at half-maximum in-plane.
Data analysis. PET images were visually interpreted and analysed
using all available clinical data and results of other imaging mo-
dalities. Any foci of FDG uptake that were increased relative to
the background and were not located in areas of physiologically
increased uptake were considered to be positive for lymphoma
lesions. A negative result was defined as no pathological FDG up-
take at any site, including all sites of previously increased patho-
logical uptake. Before and after therapy, disease was evaluated site
by site for the involved lymph nodes and organs.
For quantitative analysis of regional FDG uptake in tumour,
we calculated the standardised uptake value (SUV). In a baseline
PET study, the SUV was measured in the lesion with the highest
FDG uptake among all the positive lesions. Small, square, approx-
imately 1.0×1.0-cm regions of interest (ROIs) were defined in the
slice displaying the highest tumour activity concentration and the
neighbouring planes. The SUV represents the average radioactivi-
ty concentration of each set of three ROIs normalised for injected
dose and body weight. In the PET study after 1–2 cycles of che-
motherapy, SUV was measured in the same lesion as in the base-
line study. When the hot lesion had disappeared on the second
scan, ROIs were carefully defined in the same areas as on the
baseline scan. To evaluate the early effect of chemotherapy, we
calculated the percent reduction in SUV from the baseline value.
Clinical evaluation. Follow-up of progression-free survival (PFS)
for 24 months was related to PET results at baseline and after 1–2
cycles of chemotherapy. PFS was defined as the interval without
progression of disease from the start of chemotherapy. The
achievement of complete response was determined by a combina-
tion of clinical findings and results of imaging modalities such as
CT and magnetic resonance (MR) imaging. Complete response
was defined as complete disappearance of clinical findings and ab-
normal results of the imaging modalities, for a period of a mini-
mum of 4 weeks.
Statistical analysis. FDG-PET data were compared using an un-
paired t test. A two-sided P value <0.05 was considered significant.
Results
Table 1 shows the characteristics of the patients, includ-
ing tumour histology, staging and the International Prog-
nostic Index (IPI). Of the 20 patients studied, ten showed
24
Table 1. Patient characteristics

Patient no. Histology Stage IPI PET after 1–2 cycles Clinical outcome PFS (mo)

Responders
1 HL IIIB 2 Negative CR 28
2 DL IV 4 Negative CR 24
3 DL IV 2 Negative Relapse 10
4 DL IV 3 Negative Relapse 8
5 DL IV 4 Positive CR 34
6 DL IV 4 Positive CR 25
7 HL IIB 1 Positive Relapse 11
8 AILD T-cell III 4 Positive Relapse 8
9 DL IV 3 Positive Relapse 8
10 HL IIIB 1 Positive Relapse 16
Non-responders
11 ATL III 3 Positive PD 0
12 DL III 4 Positive PD 0
13 AILD T-cell IV 4 Positive PD 0
14 DL IV 5 Positive PD 0
15 Peripheral T-cell IV 2 Positive PD 0
16 DL II 1 Positive PD 0
17 Peripheral T-cell IV 3 Positive PD 0
18 AILD T-cell II 1 Positive PD 0
19 AILD T-cell III 1 Positive PD 0
20 DL II 1 Positive PD 0

HL, Hodgkin’s lymphoma; DL, diffuse large B-cell lymphoma; AIDL T-cell, angioimmunoblastic T-cell; ATL, adult T-cell lymphoma;
IPI, International prognostic index; CR, complete remission; PD, progressive disease; PFS, progression-free survival

Fig. 1A–F. Patient no. 18. T1-weighted coronal MR image (A)
showed an enlarged lymph node (arrow) in the right neck. Intense
FDG uptake (SUV=3.7) was observed in the transaxial PET image
(B), corresponding to the lymphadenopathy. The size of the lymph
node decreased to normal (less than 1 cm) after two cycles of che-
motherapy (C) and remained unchanged at the end of therapy (D).
Tumour FDG uptake decreased after two cycles of therapy (E) but
had risen again by the end of treatment (F), indicating progressive
disease. The percent reduction in SUV after two cycles of therapy
was 52.7%. This patient underwent additional radiation therapy

European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 1, January 2004
 25
Fig. 2. Patient no. 5. Whole-
body PET image (A) showed
multiple hot lesions in the right
chest wall (arrow) and left
shoulder (arrowhead). The
maximal tumour uptake
(SUV=17.2) was observed in
the right anterior chest wall
(arrow) on the transaxial PET
image (B). After two cycles of
chemotherapy, tumour FDG
uptake was significantly de-
creased but still showed residu-
al activity (C). Tumour SUV
was 2.1 and the percent reduc-
tion in SUV was 87.8%. This
patient achieved complete re-
mission at the end of treatment
and has been free from recur-
rence (PFS=34 months)

complete remission (CR) at the completion of chemo-
therapy while the other ten never achieved CR during the
course of therapy. Of the ten responders, four are still in
CR (PFS=24–34 months) while six have experienced
disease relapse after therapy (PFS=8–16 months). There
was no significant difference in tumour staging and IPI
between the responders and non-responders.
Visual analysis of PET
At baseline PET study, all 20 patients showed abnormal
FDG uptake in multiple sites. Four patients showed neg-
ative PET findings after 1–2 cycles of chemotherapy and
continued to be in CR at the completion of therapy (Ta-
ble 1). Two of the four patients are still in CR (PFS=24,
28 months) but the other two have relapsed after chemo-
therapy (PFS=8, 10 months). Sixteen patients had residu-
al abnormal FDG uptake after 1–2 cycles of chemothera-
py. Although six patients achieved CR at the completion
of therapy, ten showed progressive disease in spite of
chemotherapy (PFS=0 months) (Fig. 1). Two of the six
patients are still in CR (PFS=25, 34 months) (Fig. 2)
while the other four relapsed later in clinical follow-up
(PFS=8–16 months). Overall, the sensitivity, specificity
and accuracy of FDG-PET after 1–2 cycles of chemo-
therapy for the prediction of 24-month outcome were
87.5% (14/16), 50% (2/4) and 80% (16/20), respectively.
The positive and negative predictive values of PET were
87.5% (14/16) and 50% (2/4), respectively. Of the six
patients who responded to therapy but relapsed later,
four showed recurrent disease at the original sites of in-
volvement and two had recurrence at different sites.
Quantitative analysis of PET
At baseline study, the group of ten responders had a
moderately but significantly higher SUV than the group
of ten non-responders (11.3±4.2 vs 7.1±4.2, P=0.042).
After 1–2 cycles of therapy, the group of responders
showed a significantly lower SUV as compared to the
group of non-responders (1.9±0.8 vs 4.3±1.9, P=0.001)
(Fig. 3). In addition, the percent decrease in SUV from
the baseline value was significantly higher in the re-
sponders than in the non-responders (81.2%±9.5% vs
35.0%±20.2%, P<0.001) (Fig. 4). Using 60% reduction
as a cut-off value, the group of responders was clearly
separated from the group of non-responders, with the ex-
ception of one non-responder. In this non-responder, the
SUV was 17.8 at baseline and 4.7 after one cycle of ther-
apy, corresponding to a 73.6% decrease in SUV.
Discussion
Conventional chemotherapy regimens for aggressive, ad-
vanced stage NHL and HL currently result in less than
50% prolonged disease-free survival rates. At present,
high-dose chemotherapy followed by stem cell trans-

European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 1, January 2004
26
Fig. 3. Comparison of SUV after 1–2 cycles of chemotherapy be-
tween the groups of responders and non-responders
plantation is the treatment of choice for patients with re-
lapsed aggressive lymphoma who are still responding to
chemotherapy [21]. Previous studies have demonstrated
that patients with rapid response to induction treatment
are likely to have a better and more durable response
[22, 23]. Thus, accurate assessment of response early
after a course of chemotherapy is essential in order
to identify patients who may require consolidation or
salvage treatment while avoiding overtreatment and un-
necessary morbidity in those with a good prognosis.
Monitoring of chemotherapy is generally performed
by sequential determinations of tumour size using mor-
phological imaging modalities such as CT and MR imag-
ing. Based on morphological criteria alone, however, re-
sidual tumour mass cannot be differentiated from scar
tissue [4]. Moreover, tumour volume reduction measured
by CT is only a late sign of effective therapy [24]. When
CT findings are used for early therapy monitoring, a sig-
nificant number of patients may be judged as poor re-
sponders and exposed to more intensive therapy, even if
they can achieve complete response during the course of
initial therapy. 67Ga scintigraphy, using the metabolic
characteristics of tissue to detect residual tumour activi-
ty, has been shown to be useful for monitoring response
[8]. However, it has some disadvantages as compared
European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 1, January 2004
Fig. 4. Comparison of percent reduction in SUV after 1–2 cycles
of chemotherapy between the groups of responders and non-
responders
with FDG-PET imaging, in particular inferior imaging
resolution and worse interpretation of the abdomen.
In the present study, FDG-PET was performed on 20
patients with aggressive NHL or HL at baseline and after
1–2 cycles of chemotherapy to evaluate the predictive
value of FDG-PET when performed early during chemo-
therapy. In visual analysis, all four patients with negative
PET findings after 1–2 cycles remained in complete re-
mission at the completion of chemotherapy. Of the 16
patients with residual uptake after 1–2 cycles, six
achieved complete remission while the other ten showed
no response during the course of treatment (Table 1).
Accordingly, PET performed after 1–2 cycles showed
100% sensitivity (10/10) and negative predictive value
(4/4) for predicting the outcome at the completion of
therapy, but the specificity (40%, 4/10) and positive pre-
dictive value (62.5%, 10/16) were relatively low. In
quantitative analysis, tumour SUVs after 1–2 cycles of
therapy were significantly lower in the group of respond-
ers than in the group of non-responders (Fig. 3). In addi-
tion, using 60% reduction in SUV as a cut-off value, the
group of responders could be clearly separated from the
group of non-responders, with the exception of one non-
responder (Fig. 4). These results suggest that PET ob-
tained early during chemotherapy may have a high prog-

nostic value for evaluation of therapy and that quantita-
tive analysis seems to be more useful for predicting re-
mission status at the completion of chemotherapy than
visual analysis.
For predicting the long-term outcome (24 months),
visual analysis of FDG-PET after 1–2 cycles of chemo-
therapy showed a sensitivity and a positive predictive
value of 87.5% (14/16), but the specificity was only 50%
(2/4), as compared with a specificity of 87% for predict-
ing the 18-month outcome in the study of Kostakoglu et
al. [17]. The latter authors evaluated the predictive value
of FDG-PET after one cycle of therapy for clinical out-
come in 30 patients with aggressive lymphoma. The dis-
crepancy between their results and ours may partly de-
rive from differences in the patient population, treatment
protocols and length of follow-up. Another possible ex-
planation is the difference in the PET imaging equipment
employed. Kostakoglu et al. used a dual-head gamma
camera operated in coincidence mode while we used a
dedicated full-ring PET camera. The sensitivity of coin-
cidence PET scanners is well known to be inferior to that
of dedicated PET scanners. In previous studies [18, 19],
coincidence gamma camera showed poor sensitivity for
lesions clearly detected at dedicated FDG-PET in the ab-
domen and elsewhere; this was especially evident for le-
sions smaller than 1.5 cm. Thus, it may be assumed that
a coincidence camera, with poor sensitivity, could fail to
detect small residual disease after one cycle of therapy—
such failure would have resulted in overestimation of
specificity and negative predictive value in the study by
Kostakoglu et al.
In order to predict the clinical response early during
chemotherapy, Romer et al. performed dynamic FDG-
PET studies on 11 lymphoma patients at baseline and at
7 days (one cycle) and 42 days (two cycles) after the initi-
ation of therapy [25]. During a follow-up of 16±4 months,
six of the 11 patients continued to show complete remis-
sion. In this study, tumour FDG uptake at 42 days after
therapy was superior to that after 7 days for the predic-
tion of long-term outcome. At day 42, a significantly
lower FDG metabolic rate and significantly lower SUVs
were observed in the group of responders, as compared
with the group of relapsed patients. The authors conclud-
ed that kinetic parameters are more sensitive metabolic
signals to chemotherapeutic interventions than SUV pa-
rameters; however, dynamic PET imaging and kinetic
analysis may be complicated and time consuming in rou-
tine clinical work.
High-dose chemotherapy is increasingly performed in
patients who respond to conventional chemotherapy, and
there is some evidence that patients who receive such
therapy early after achieving a remission to first-line
therapy have a higher rate of cure [26]: hence the impor-
tance of establishing the remission status as early as pos-
sible. In this clinical setting, our data demonstrate that
FDG-PET obtained early after chemotherapy may sepa-
rate patients with a good prognosis who can be cured
European Journal of Nuclear Medicine and Molecular Imaging Vol. 31, No. 1, January 2004
27
with standard therapy from those with a poorer progno-
sis, in whom more aggressive treatment may be required.
Mikhaeel et al. [27] found that an interim FDG-PET scan
after 2–3 cycles of chemotherapy may predict the long-
term freedom from relapse more accurately than the
post-treatment PET scan. A prospective study is war-
ranted to determine whether patients who change or do
not change treatment based on PET results early during
therapy will achieve a better outcome.
Our study may have a shortcoming in that the trial pa-
tients had different diseases and thus were being treated
differently. It would have been difficult to analyse the
patients separately according to tumour histology or
staging because the groups would have become very
small. Further studies and more data would be necessary
to solve this problem.
In conclusion, in patients with aggressive lymphoma,
FDG-PET performed early during chemotherapy may
offer important prognostic information on clinical
outcome and allow the differentiation of responders
from non-responders. Larger prospective studies are
necessary to confirm these findings and to establish the
role of FDG-PET in the management of lymphoma
patients.
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