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The use of deauville criteria in follow up assessment of response to therapy in extra-nodal non-hodgkin's lymphoma
1. Contents lists available at ScienceDirect
The Egyptian Journal of Radiology and Nuclear Medicine
journal homepage: www.elsevier.com/locate/ejrnm
Original Article
The use of Deauville criteria in follow-up assessment of response to therapy
in extra-nodal Non-Hodgkin's lymphoma
Manar Hussein Abdel-Sattara
, Omar Abdelaziza,ā
, Amr Othman Othmanb
,
Sherief Mohamed El-Refaeic
a
Diagnostic and Interventional Radiology Department, Cairo University Hospitals, Cairo, Egypt
b
Radiology Department, Shoubra General Hospital, Cairo, Egypt
c
Nuclear Medicine Department, Cairo University Hospitals, Cairo, Egypt
A R T I C L E I N F O
Keywords:
PET/CT
Extranodal non-hodgkin lymphoma
Deauville criteria
IHP (International Harmonizing Project)
A B S T R A C T
Objective: Our aim was evaluate the role the PET/CT in the assessment of response to therapy in patients with
Non-Hodgkin extra-nodal lymphoma: in particular, a ļ¬ve-point scale (Deauville criteria), which can be em-
ployed for early- and late-therapeutic response assessment.
Methods: Sixty patients with pathologically conļ¬rmed Non-Hodgkin lymphoma (NHL) were enrolled in this
prospective study. All patients underwent the following PET/CT examinations: initial PET/CT for staging, in-
terim PET/CT and end of treatment PET/CT. Response assessment was done using new Chesonās guidelines and
ļ¬ve-point scale (Deauville criteria).
Results: All patients were evaluated for response to therapy in the early interim, followed by late interim, as well
as end treatment assessment for the overall response. We found good concordance of response assessment ac-
cording to the Deauville criteria classiļ¬cation with International Harmonization Project (IHP) classiļ¬cation.
After early interim 48/60 patients had concordant designations (91.7%, 83.3%, 70%, and 33.3%) and 12 pa-
tients had discordant designations. After late interim, 56/60 patients had concordant designations (100%, 100%,
80%, and 50%) and four patients had discordant designations. After end of treatment, 54/60 patients had
concordant designations (100%, 100% and 71.4%) and six patients has discordant designations.
Conclusion: Response assessment according to the Deauville criteria classiļ¬cation showed good concordance
with IHP classiļ¬cation. According to our ļ¬ndings, we recommend the use of Deauville criteria in reporting of
PET/CT for staging and assessment of response to treatment.
1. Introduction
Lymphoma is the most frequent primary hematopoietic malignancy.
Non-Hodgkin lymphoma accounts for approximately 5% of all cases of
cancer with greater predilection to disseminate to extra-nodal sites [1].
The extra-nodal involvements are compromising in approximately
40% of patients. The term extra-nodal involvement refers to lympho-
matous inļ¬ltration of anatomic sites aside from the lymph nodes [2]. It
is due to the regional spread of nodal disease or blood dissemination
[3].
The advantage of metabolic imaging is its ability to distinguish vi-
able metabolically active tissue from scars. Additionally, it has the
potential to detect functional changes in response to chemo- or radio-
therapy before any change in clinical or radiological size of a mass
occurs [4].
Assessment of response to treatment is considered one of the most
important issues in lymphomas imaging. How to diļ¬erentiate ļ¬brosis
from viable tumor within residual masses, represents a dilemma of in-
terpretation for lymphomatous lesions. Therefore, accurate staging is
critical for the selection of a proper therapeutic approach, in order to
prevent further un-needed treatment, and to lessen morbidity caused by
the therapy applied [5].
The most common response evaluation guideline in lymphoma was
carried out as per the International Workshop Criteria (IWC, 1999)
guidelines and revised response criteria by International Harmonization
Project (IHP) [6].
The aim of this work was to evaluate the role the PET/CT in the
assessment of response to therapy in patients with Non-Hodgkin extra-
nodal lymphoma: particularly, a ļ¬ve-point scale (Deauville criteria) to
grade response utilizing PET/CT.
https://doi.org/10.1016/j.ejrnm.2017.10.010
Received 14 February 2017; Accepted 27 October 2017
Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine.
ā
Corresponding author at: Diagnostic and Intervention Radiology Department, Cairo University Hospitals, El-Manial, 11956 Cairo, Egypt.
E-mail address: ohamada@yahoo.com (O. Abdelaziz).
The Egyptian Journal of Radiology and Nuclear Medicine 49 (2018) 209ā215
Available online 28 March 2018
0378-603X/ copyright 2018 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/BY-NC-ND/4.0/).
T
2. 2. Patients and methods
The study was performed in a private Radiology centre, and all
patients agreed to participate in the study. During two years duration,
we prospectively evaluated 60 patients with pathologically conļ¬rmed
NHL. This study included 44 males and 16 females, ranging in age from
20 and 78 years old (mean age 51 Ā± 17.4 years). Patients underwent
the following PET/CT examinations: initial PET/CT for staging, interim
PET/CT and end of treatment PET/CT.
2.1. Imaging protocol
All examinations were acquired using a combined PET/CT in-line
system (Syngo PET VG 50A Biograph 20 VA 44A, Siemens Medical
Solutions, Berlin, Germany). All patients administered one liter of ne-
gative oral contrast agent (5% mannitol) approximately one hour be-
fore the examination. 370ā555 MBq (10ā20 mCi) (3ā5 MBq/kg) 18F-
FDG was IV administered 45ā90 min prior to the examination.
First non contrast low dose CT images were obtained. This was
followed by whole body PET scan in 3D mode. Lastly, a diagnostic
contrast-enhanced CT scan was obtained with an application of 100 mL
nonionic contrast agent (Optiray 350 [Ioversol 74%], Covidien,
Germany) in porto-venous phase (70 s delay). The whole acquisition
time for an integrated PET/ CT scan was approximately 25 min.
2.2. Timing of exam
Post-therapy PET/CT examinations were performed not less than
4ā6 weeks after surgery or chemotherapy and 8ā12 weeks after external
beam radiation therapy or radio-immunotherapy. These intervals
minimize the chances of false-negative (FN) and false-positive (FP)
ļ¬ndings.
2.3. PET/CT interpretation
All PET/CT examinations were analyzed by two experienced ob-
servers (Radiologist and nuclear medicine specialist). The PET images
and the volume of CT scans were assessed for the existence and extent
of 18F-FDG-positive lymphoma in diļ¬erent lymph node groups, the
presence of extra-nodal lymphomatous inļ¬ltrates, as well as the pre-
sence of non FDG avid residual soft-tissue abnormalities.
Patients were staged according to the Ann Arbor classiļ¬cation [7].
Response assessment was performed using new Chesonās guidelines
(Table 1) [6] and ļ¬ve-point scale (Deauville criteria) (Table 2) [5].
FDG avid residual masses of 2 cm or more with maximum SUV ex-
ceeding that of mediastinal structures are considered PET positive,
whereas masses 1.1ā1.9 cm are considered PET positive only if their
metabolic activity is higher than the surrounding background activity.
A smaller residual mass or a normal-sized lymph node (e.g. < 1
Ć 1 cm) should be considered positive for disease if its activity is
higher than that of the surrounding background.
Diļ¬use splenic involvement was diagnosed when the splenic activity
exceeded that of the liver. Splenic or hepatic lesions which are larger
than 1.5 cm on CT should be considered as positive lymphomatous le-
sion if their uptake is higher than or equal to that of the liver or spleen.
If there was a diļ¬usely increased FDG uptake of the bone marrow,
the patient was considered as PET positive. Diļ¬use FDG uptake after
chemotherapy, can be due to reactive bone marrow hyperplasia, con-
sequently, thorough history taking was essential. A delay of 3ā4 weeks
after end of therapy permits the physiologic marrow activity to abate
[8].
3. Results
On the basis of the IHP after early interim, 24 patients had a com-
plete response (CR), 10 had progressive disease (PD), 20 had a partial
response (PR) and 6 had stable disease (SD). In comparison, on the basis
of Deauville criteria, 26 patients had a CR, 12 had PD, 18 had a PR and
four had SD (Table 3). Overall, 48 out of 60 patients had concordant
Table 1
Criteria of therapeutic response by international harmonization project (IHP) [6].
Response Deļ¬nition Nodal masses Spleen and liver Bone marrow
Complete response No evidence of disease Previously enlarged FDG-avid lymph nodes size
decreased to normal (ā¤1.5 cm)
Diminution in size, and
disappearance of nodules
No inļ¬ltrate at repeat biopsy
Partial response Regression of disease and no
newly developed sites
ā„50% diameter decrease of up to six of the largest
masses, no increase in size of other nodes
ā„50% decrease in size of
nodules
Irrelevant if ļ¬ndings are positive
before therapy, the type of cell
should be speciļ¬ed
Stable disease Failure to attain CR/PR or
PD
PET positive at previous sites of disease and no
new sites at CT or PET
Relapse or progressive
disease
Newly developed lesions or
increase by 50% of previous
lesions
Appearance of one or more new lesions > 1.5 cm,
ā„50% increase in size of more than one node; new
FDG-avid lesions
> 50% increase in size of
any previous lesions
New or recurrent involvement
Table 2
Criteria of therapeutic response by Modiļ¬ed Deauville Criteria [5].
Score PET/CT scan result
1 No uptake above background
2 Uptake at an initial site that is lower than or equal to mediastinum
3 Uptake at an initial site that is more than mediastinum but lower than or
equal to liver
4 Uptake at an initial site that is moderately increased in comparison to the
liver
5 Uptake at an initial site that is markedly increased in comparison to the
liver
Table 3
Response designations according to the IHP and Deauville criteria classiļ¬cations after early interim treatment.
IHP after early interim
CR (n = 24) PD (n = 10) PR (n = 20) SD (n = 6)
Deauville after early interim CR (n = 26) 22 (91.7%) 0 (0%) 4 (20.0%) 0 (0%)
PD (n = 12) 0 (0%) 10 (83.3%) 0 (0%) 2 (33.3%)
PR (n = 18) 2 (8.3%) 0 (0%) 14 (70.0%) 2 (33.3%)
SD (n = 4) 0 (0%) 0 (0%) 2 (10.0%) 2 (33.3%)
M.H. Abdel-Sattar et al. The Egyptian Journal of Radiology and Nuclear Medicine 49 (2018) 209ā215
210
3. Table 4
Response designations according to the IHP and Deauville criteria classiļ¬cations after late interim treatment.
IHP after late interim
CR (n = 26) PD (n = 20) PR (n = 10) SD (n = 4)
Deauville after late interim CR (n = 26) 26 (100%) 0 (0%) 0 (0%) 0 (0%)
PD (n = 22) 0 (0%) 20 (100%) 0 (0%) 2 (50.0%)
PR (n = 8) 0 (0%) 0 (0%) 8 (80%) 0 (0%)
SD (n = 4) 0 (0%) 0 (0%) 2 (20%) 2 (50%)
Table 5
Response designations according to the IHP and Deauville criteria classiļ¬cations after end 0f treatment.
IHP after end 0f treatment
CR (n = 34) PD (n = 10) PR (n = 14) SD (n = 2)
Deauville after end of treatment CR (n = 34) 34 (100%) 0 (0%) 0 (0%) 0 (0%)
PD (n = 16) 0 (0%) 10 (100%) 4 (28.6%) 2 (100%)
PR (n = 10) 0 (0%) 0 (0%) 10 (71.4%) 0 (0%)
Data are expressed as number (percent).
Fig. 1. 43 year-old male patient. (a) In the pretreatment evaluation, there is metabolically active disease involving multiple lymph nodes above and below the
diaphragm, liver, spleen and bone marrow with soft tissue intermuscular nodules, the patient were staged IVS with Deauville criteria score 5. (b) After 3 cycles
chemotherapy (early interim response), there is complete metabolic response of the nodal, hepatic and splenic disease and partial metabolic response of the bone
marrow lesions. Corresponding Deauville criteria score 4. (c) After end of treatment, PET/CT showed no FDG-avid lesions distinctive for active lymphoma or
recurrent disease, corresponding Deauville criteria score 2. Overall response by Deauville criteria showed concordance with IHP.
M.H. Abdel-Sattar et al. The Egyptian Journal of Radiology and Nuclear Medicine 49 (2018) 209ā215
211
4. designations (91.7%, 83.3%, 70%, and 33.3%) and 12 patients had
discordant designations.
After late interim, on the basis of the IHP, 26 patients had a CR, 20
had PD, ten had a PR and four had SD. In comparison, by the basis of
Deauville criteria, 26 patients had a CR, 22 had PD, eight had a PR and
four had SD (Table 4). Overall, 56 out of 60 patients had concordant
designations (100%, 100%, 80%, and 50%) and four patients had dis-
cordant designations.
On the basis of the IHP after end of treatment, 34 patients had a CR,
ten had PD, 14 had a PR and two patients had SD. In comparison, by the
basis of Deauville criteria, 34 patients had a CR, 16 had PD, ten had a
PR and no patient had SD (Table 5). Overall, 54 out of 60 patients had
concordant designations (100%, 100% and 71.4%) and six patients has
discordant designations (Figs. 1ā4).
4. Discussion
One of the most challenging aspects in the imaging of lymphoma is
the evaluation of response to treatment. Diļ¬erentiation of active lesions
represents a problem of interpretation for Non-Hodgkin lymphoma.
Thus accurate staging is considered the best mean for the choice of a
proper therapeutic approach, in order to prevent over or under treat-
ment as well as to minimize morbidity related to the radio-che-
motherapy regimens given [5].
Using CT to monitor changes in lymph nodes size was the main basis
of evaluation of therapeutic response. However, it was diļ¬cult to
Fig. 2. 30 years old male patient. (a) In the pretreatment evaluation, there is wide spread metabolically active nodal and extra nodal (bone marrow) as well as splenic
lesions, the patient were staged IVS with Deauville criteria score 5. (b) After 3 cycles chemotherapy (early interim response) there is marked metabolic regression of
the previously noted lymph nodal and bone marrow disease. Complete metabolic resolution of the previously noted splenic lesions. Corresponding Deauville criteria
score 4. (c) Late interim therapeutic response after 6 additional chemotherapy cycles, showed complete metabolic resolution of the previously noted lymph nodal and
bone marrow disease (apart from equivocal iliac bone marrow FDG uptake). Re-demonstrations of two hypermetabolic splenic focal lesions denoting recurrence
splenic aļ¬ection. Newly developed right lung hypermetabolic acinar changes are likely inļ¬ammatory. Corresponding Deauville criteria score 4. (d) The patient
received additional 3 cycles in a total of 12 cycles and came for end of treatment therapeutic response, PET/CT showed metabolic and morphological progression of
the hypermetabolic splenic and iliac bone lymphomatous lesions. Newly depicted metabolically active multiple splenic and lymph nodal lesions, keeping with disease
progression. Total resolution of right lung consolidative patch, corresponding Deauville criteria score 5. Overall response by Deauville criteria showed concordance
with IHP.
M.H. Abdel-Sattar et al. The Egyptian Journal of Radiology and Nuclear Medicine 49 (2018) 209ā215
212
5. distinguish post-treatment ļ¬brosis from residual viable tissue. PET/CT,
with its improved potential in diļ¬erentiating benign ļ¬brosis (absent or
low-grade 18F-FDG uptake) and residual active lymphoma (elevated
18F-FDG uptake) has been found helpful in assessment of therapeutic
response [9].
In this study, we evaluated patients for response to therapy in the
early interim assessment, following one to three cycles of treatment,
late interim assessment and end treatment assessment of the overall
response, usually performed approximately one month after termina-
tion of chemotherapy. An early assessment of patients who responded
to therapy is particularly helpful in malignancies for which there could
be diļ¬erent chemotherapeutic regimens. Additionally, early assessment
can help to prevent unnecessary side eļ¬ects as well as reduces cost and
morbidity [10].
There are diļ¬erent methods for the assessment of radiotracer (18F-
FDG) uptake by normal and pathologic tissues, including visual in-
spection and the standardized uptake value (SUV) [11].
The CT portion of PET/CT exams is pivotal in the response eva-
luation of lymphoma patients. Following the IHP criteria, if residual
metabolic activity associated with morphological reduction is dis-
covered, the response is either PR or SD, determined by how much
reduction in size is reported by CT (i.e. if the reduction in size was
Fig. 3. 67 years old female patient. (a) In the baseline study evaluation, there is wide spread metabolically active nodal as well as splenic lesions, the patient were
staged IVS with Deauville criteria score 5. (b) In the interim response after 8 cycles of chemotherapy thereās two newly observed hypermetabolic lymph nodes in the
apex of the left axilla, suggestive of metabolically active disease (progressive disease). Complete metabolic and morphologic resolution of almost all lymphade-
nopathy. Corresponding Deauville criteria score 3. (c) After end of treatment, PET-CT showed metabolic and morphological progression of the lymph nodes above
and below the diaphragm. Marked disease progression regarding the extranodal disease with newly depicted splenic, right lung, left kidney, left adrenal and multiple
soft tissue nodules ācutaneous, muscular and inter-muscularā, corresponding Deauville criteria score 5. Overall response by Deauville criteria showed concordance
with IHP.
M.H. Abdel-Sattar et al. The Egyptian Journal of Radiology and Nuclear Medicine 49 (2018) 209ā215
213
6. by > 50%, it is considered PR while if the reduction was by ā¤50%, it is
considered SD). Consequently, CT is extremely valuable in diļ¬er-
entiating patients with PR from those with SD, thus sparing the patients
with PR from more aggressive treatment, while the patients with SD
may beneļ¬t from modifying the treatment regimen [6].
In our study, visual assessment using Deauville criteria were used to
assess diļ¬erent degrees of response at interim and after termination of
treatment. Interpretation of the PET/CT ļ¬ndings in this study corre-
sponded with the results of Yang et al. [12]; it was qualitative and semi-
quantitative. The qualitative evaluation (visual) included the descrip-
tion of all the hypermetabolic lesions (activity > liver) deļ¬ned as
positive scan that attain focal or diļ¬use FDG uptake above background.
The semi-quantitative evaluation or SUV based evaluation was per-
formed using the maximum standardized uptake value (SUV max) in a
region of interest located over the hypermetabolic lesion. The reduction
in metabolic activity of the lesions was quantiļ¬ed using the percentage
of reduction of SUV max [12].
SUV is a simpliļ¬ed index of 18F-FDG uptake, it is a ratio that can be
understood as the concentration of 18F-FDG within a lesion, divided by
the concentration of radiotracer distributed throughout the body [13].
Previous studies reported high prognostic value of interim PET/CT
A precise timely prediction of the response to therapy could help to
select patients who might be cured with conventional therapy from
patients for whom an early change to alternative, more aggressive
treatment approaches are required [14]. In this study, patients with
persistent disease at the end of treatment had interim PET/CT positive
results, while not all the patients with interim PET/CT negative results
end in CR after completion of treatment, disease relapse is not un-
common.
On interpretation of PET/CT at early interim after one to three cy-
cles of chemotherapy: according to the IHP, 24 patients had a CR, 10
had PD, 20 had a PR and six had SD. In comparison, by the basis of
Fig. 4. 38 years old male patient. (a) In the baseline study evaluation, there is evidence of hypermetabolic lymphadenopathy above the diaphragm at the cervical and
right axillary lymph node groups. Additionally, a sclerotic right iliac bone lesion and few pulmonary nodules show metabolic activity. The patient were staged IV
with corresponding Deauville criteria score 5. (b) In the interim response, there is metabolic regression of the previously noted FDG avid left cervical and right
axillary lymph nodes. Complete metabolic resolution of the right iliac bone lesion. Newly developed low grade metabolic activity within right cervical, anterior
mediastinal, para-aortic and right inguinal lymphadenopathy. Stable appearance regarding the right pulmonary nodule. Corresponding Deauville criteria score 5. (c)
After end of treatment, PET/CT showed complete metabolic and morphologic remission of the nodal and extranodal disease with no current metabolically active
lymphoma. Overall response by Deauville criteria showed concordance with IHP.
M.H. Abdel-Sattar et al. The Egyptian Journal of Radiology and Nuclear Medicine 49 (2018) 209ā215
214
7. Deauville criteria, 26 patients had a CR, 12 had PD, 18 had a PR and
four had SD. Overall, 48/60 patients had concordant designations
(91.7%, 83.3%, 70%, and 33.3%) and 12 patients had discordant des-
ignations.
Our study agreed with Hutchings et al. [15] which reported that
18F-FDG PET after one to three cycles of chemotherapy for NHL was
highly predictive of the ļ¬nal treatment response. Further, this corre-
sponds with the study conducted by Strobel et al. [16] which reported
that 31 out of 38 NHL patients showed CR in interim PET/CT exams and
all remained 18F-FDG negative in the end-treatment PET/CT.
Previous studies reported that persistent 18F-FDG uptake after two
to four cycles of chemotherapy was associated with poor prognosis
[9,17,18].
On interpreting PET/CT at late interim after more than three cycles
of chemotherapy, we found good concordance of response assessment
according to the Deauville criteria classiļ¬cation with IHP classiļ¬cation.
Only four patients had discordant designations, whereas 56/60 patients
had concordant designations (100%, 100%, 80%, and 50%).
Also, there was good concordance of response assessment according
to the Deauville criteria classiļ¬cation with IHP classiļ¬cation when
evaluating patients after end treatment. Overall, 54/60 patients had
concordant designations (100%, 100% and 71.4%) and six patients has
discordant designations.
Similar to the ļ¬ndings of the previous studies conducted by Itti et al.
and Evens and Kostakoglu [18,19], we found that response assessment
according to the Deauville criteria classiļ¬cation appears to have good
concordance with the IHP classiļ¬cation in treatment response assess-
ment.
An interim PET scan could be used to determine whether to escalate
or deescalate therapy, based on whether a scan is positive or negative. A
score of 1 to 5 based on Deauville criteria categorizes patients as PET-
negative or PET-positive. When dose intensiļ¬cation is planned, a
Deauville score of 1 to 3 is regraded as PET-negative and a score of 4 to
5 is regraded as PET-positive; those who are PET-negative will not re-
quire more intensive therapy. However, if dose deescalation is planned,
scores of 1 to 2 are considered PET negative and 3 to 5 PET-positive.
These shifts in score categories were designed to avoid over-treatment
and under- treatment [20].
5. Conclusion
Response assessment according to the Deauville criteria classiļ¬ca-
tion appears to have good concordance with the IHP classiļ¬cation in
treatment response assessment and intended to represent a practical
framework used for interim PET/CT follow up of Non Hodgkin
Lymphoma.
Conļ¬ict of interest
The authors declared no conļ¬ict of interests.
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