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Japanese Journal of Clinical Oncology, 2019, 149(10)895–900

doi: 10.1093/jjco/hyz111
Advance Access Publication Date: 28 August 2019
Review Article

Review Article

Revised staging system for malignant


lymphoma based on the Lugano classification
Wataru Munakata1 ,*, Takashi Terauchi2 , Dai Maruyama1 , and

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Hirokazu Nagai3
1
Department of Hematology, National Cancer Center Hospital, Tokyo, Japan, 2 Department of Nuclear Medicine,
Cancer Institute Hospital, Japanese Foundation for Cancer Research, Tokyo, Japan, and 3 Clinical Research Center,
National Hospital Organization Nagoya Medical Center, Nagoya, Japan

*For reprints and all correspondence: Wataru Munakata, Department of Hematology, National Cancer Center Hospital, 5-1-1
Tsukiji, Chuo-ku, Tokyo 104-0045, Japan. E-mail: wmunakat@ncc.go.jp
Received 21 March 2019; Accepted 2 July 2019

Abstract
The Lugano classification was published in 2014 to form the basis for revising the recommendations
regarding anatomic staging and evaluation of disease before and after therapy. This staging
system was adopted by the eighth edition of the Cancer Staging Manual of the American Joint
Committee on Cancer. In this review, we aimed to discuss this updated staging system for
malignant lymphomas. The most important change was that fluorodeoxyglucose positron emission
tomography/computed tomography became the new standard imaging technique for staging of
all fluorodeoxyglucose-avid histologies. Due to the introduction of fluorodeoxyglucose positron
emission tomography/computed tomography for staging, the evaluation of not only lymph node
involvement but also organ involvement, including liver or spleen, has become simplified. Further-
more, it is possible to eliminate bone marrow biopsies in patients with Hodgkin lymphoma and
diffuse large B-cell lymphoma. Although patients were grouped according to the absence (A) or
presence (B) of disease-related symptoms based on the previous classification, only the patients
with Hodgkin lymphoma need to be assigned the designations A or B in this revision. Hopefully,
these revised recommendations will improve patient management and the conduct of clinical trials.

Key words: Lugano classification, FDG-PET/CT, malignant lymphoma, AJCC

Introduction for radiation therapy. As the spread patterns of non-HL (NHL) were
A universally accepted and reproducible staging system is critical different from those of HL, the Ann Arbor classification did not seem
for the standardized management of patients with malignant lym- to be applicable to NHL. Although the Ann Arbor classification was
phomas, because clinical staging plays a more significant role in the originally intended for staging of with HL, it has also become the
selection of patients’ treatment than any other clinical factors, and only widely used staging system for NHL.
clinical stage is one of the factors that can be used to predict the As the imaging technologies and treatment modalities were
prognosis of diseases. The Ann Arbor classification became the first improved, the original staging system was updated as the Cotswold
widely accepted stating system for lymphoma since 1971. The Ann Modification to address some of the issues present in the original
Arbor classification was designed primarily for the initial evaluation staging system and to accommodate newer diagnostic techniques,
of patients with Hodgkin lymphoma (HL) (1). It was based on the including computed tomography (CT) scan (2). After introducing
relatively predictable pattern of spread of HL and can help improve Cotswold Modification of Ann Arbor classification into clinical
the ability to determine which patients might be suitable candidates practice, CT scan was recommended as the routine staging procedure,

© The Author(s) 2019. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
895
896 Revised staging system for malignant lymphoma

and staging laparotomy was only indicated in patients whom the


results would potentially change the treatment plan. These staging
system has been accepted as the standardized system to describe the
anatomic disease extent and has been useful as a universal system for
a variety of lymphomas; therefore, it was adopted by the American
Joint Committee on Cancer (AJCC) and the Union for International
Cancer Control (UICC) as the official staging system for classifying
the anatomic extent of diseases in patients with both HL and NHL.
The fluorodeoxyglucose positron emission tomography (FDG-
PET) technology was invented in 1987 and the first applied to
lymphoma assessment around 1990. As FDG-PET scan was more
beneficial than CT, as it can distinguish viable tumour from scar
and fibrosis, Dr Juweid et al. incorporated FDG-PET into the stan-
dard lymphoma response criteria (3). They noted that in patients

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with diffuse large B-cell lymphoma (DLBCL), long-term outcome
was similar regardless of whether the patient achieved a complete
response or partial response based on CT criteria, as long as the
mass was not FDG avid. Thus, complete remission unconfirmed
was eliminated as a response category. Based on the accumulated
data, the revised response criteria for malignant lymphoma were
developed and published in 2007 (4). These criteria were the first
to include FDG-PET as part of response assessment because of its
superior sensitivity and specificity compared with CT and became the
gold standard for evaluation of malignant lymphoma. By introducing Figure 1. Lymph node regions. The staging classification for malignant
these response criteria, it was expected that fewer patients would be lymphoma uses the term ‘lymph node region’. They are not based on any
either undertreated or overtreated. This 2007 International Working physiologic principles but have been used by convention.
Group recommendations were primarily designed for patients with
HL and DLBCL, because data regarding the use of FDG-PET for
evaluation of other histological subtypes were limited. Whereas extended to a non-nodal site (stage IIE). On the contrary, E suffix
FDG-PET was frequently performed at baseline prior to initiation of does not apply to patients with stage III nodal disease; any patient
treatment, it had not yet been formally incorporated into the staging with nodal disease above and below the diaphragm with concurrent
system due to the limited available data at that time. contiguous extralymphatic involvement is diagnosed with stage IV
Following the extensive use of these criteria, sufficient amount of disease (previously classified into stage IIIE).
additional information and evidence had been generated, including
data supporting the role of FDG-PET in evaluating other histological
subtypes, especially follicular lymphoma (FL). Furthermore, there Lymph node regions
was consensus regarding the use of standardized criteria for inter-
The staging classification for malignant lymphoma uses the term
pretation of scans, that is, the Deauville 5-point scale (5). At the
‘lymph node region’. The lymph node regions were defined at the
11th and 12th International Conference on Malignant Lymphoma
Rye Symposium in 1965 and have been used in the Ann Arbor
(ICML), workshops were held to study areas in need of clarification
classification. This remains unchanged in the Lugano classification
or updates of the revised staging system and then to review the
(Fig. 1). They are not based on any physiologic principles but have
proposed changes. For 2 years before the 12th ICML, imaging and
been used by convention. The currently accepted classification of
clinical subcommittees had extensive communication to reach a
core nodal regions is shown in Table 2. In addition to these core
consensus. At the 12th ICML, the Lugano classification was finally
regions, lymphomas may involve epitrochlear lymph nodes, popliteal
presented and published 1 year later (5,6). Through the extensive
lymph nodes, internal mammary lymph nodes, occipital lymph nodes,
communication between imaging and clinical subcommittees, the
submental lymph nodes, preauricular lymph nodes and many other
Lugano classification forms the basis for revising the recommenda-
small nodal areas. As clinical prognostic models, e.g. for FL (8–10) or
tions regarding anatomic staging and evaluation of disease before
localized HL (11), include specific definitions of nodal regions, which
and after the therapy. This staging system is adopted by the updated
differ from nodal regions for staging, careful attentions are needed to
AJCC. In this review, we aimed to discuss this updated staging system
evaluate prognostic factors.
for malignant lymphoma.

Revisions to staging procedure and criteria


Updated staging system from Lugano Imaging technology
classification The Lugano classification regards FDG-PET/CT as the standard
In the Lugano classification, a modification of the Ann Arbor classi- procedure for routine staging of FDG-avid histological subtypes,
fication was recommended for anatomic description of disease extent essentially all histological subtypes except for chronic lymphocytic
(Table 1) (7). The designation E for extranodal disease is applicable leukaemia/small lymphocytic lymphoma, lymphoplasmacytic lym-
only for patients with limited extranodal disease in the absence phoma, marginal zone lymphoma and mycosis fungoides (Table 3)
of nodal involvement (stage IE) or limited nodal disease directly (5). For these histological subtypes, CT scan is preferred. These
Jpn J Clin Oncol, 2019, Vol. 49, No. 10 897

Table 1. Revised staging system based on the Lugano classification

Stage Stage description

Limited stage
Stage I Involvement of a single lymphatic site
Stage IE Single extralymphatic site in the absence of nodal involvement
Stage II Involvement of two or more lymph node regions on the same side of the diaphragm
Stage IIE Contiguous extralymphatic extension from a nodal site with or without involvement of other lymph node regions on the same
side of the diaphragm
Stage II bulkya Stage II with disease bulk
Advanced stage
Stage III Involvement of lymph node regions on both sides of the diaphragm; nodes above the diaphragm with spleen involvement
Stage IVb Diffuse or disseminated involvement of one or more extralymphatic organs, with or without associated lymph node involvement;
or non-contiguous extralymphatic organ involvement in conjunction with nodal stage II disease or any extralymphatic organ

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involvement in nodal stage III disease

a
Stage II bulky may be considered either early or advanced stage based on lymphoma histology and prognostic factors.
b
Stage IV includes any involvement of the cerebrospinal fluid, bone marrow, liver or multiple lung lesions.

Table 2. The classification of core nodal regions Table 3. Fluorodeoxyglucose (FDG) avidity according to histological
subtypes
Nodal region
Histology FDG avidity (%)
Cervical nodesa Right
Left Hodgkin lymphoma 97–100
Axially nodes Right Diffuse large B-cell lymphoma 97–100
Left Follicular lymphoma 91–100
Infraclavicular nodes Right Mantle cell lymphoma 100
Left Burkitt lymphoma 100
Mediastinal lymph nodes Nodal marginal zone lymphoma 100
Hilar lymph nodes Right Lymphoblastic lymphoma 100
Left Anaplastic large cell lymphoma 94–100
Para-aortic lymph nodes NK/T-cell lymphoma 83–100
Mesenteric lymph nodes Angioimmunoblastic T-cell lymphoma 78–100
Pelvic lymph nodes Right Peripheral T-cell lymphoma, not otherwise 86–98
Left specified (NOS)
Inguinofemoral lymph nodes Right Extranodal marginal zone lymphoma of 54–81
Left mucosa-associated lymphoid tissues
(MALT lymphoma)
a
Cervical nodes include cervical, supraclavicular, occipital and preauricular Small lymphocytic lymphoma 47–83
lymph node. Enteropathy-associated T-cell lymphoma 67–100
Splenic marginal zone lymphoma 53–67
Mycosis fungoides 83–100
revised recommendations are intended for patients with primary Sézary syndrome 100
nodal involvement, although they are also applicable to patients with Primary cutaneous anaplastic large cell lymphoma 40–60
primary extranodal DLBCL. Subcutaneous panniculitis-like T-cell lymphoma 71
Although FDG-PET/CT is strongly recommended for staging of
routinely FDG-avid histological subtypes, a contrast-enhanced CT
scan is preferred to distinguish bowel from lymphadenopathy and alone, up to six of the largest target nodal or extranodal lesions
to evaluate the compression of major vessels. Furthermore, as CT that are 2 diameters in size (longest diameter [LDi] and shortest
scan identifies more hilar nodes and may better discriminate between diameter) should be identified from different body regions, which
a single large nodal mass and an aggregate of individual nodes, is representative of the patient’s overall disease burden, and should
a contrast-enhanced CT scan should be performed to accurately include mediastinal or retroperitoneal disease, if involved. A measur-
measure the nodal size especially in clinical trials. In clinical practice, able nodal and extranodal lesion must have an LDi greater than 1.5
both FDG-PET/CT and contrast-enhanced CT scan are performed and 1.0 cm, respectively. All other lesions should be followed as non-
for staging of lymphoma. measured disease. In patients with tumours of discordant histology or
Since the designation of Ann Arbor classification, nodes larger suspected of aggressive transformation, FDG-PET/CT findings may
than 1.5 cm are considered abnormal. By contrast, for patients eval- identify the optimal site for biopsy for histological confirmation.
uated with FDG-PET/CT, focal FDG uptake in nodal and extranodal
sites that can be distinguished from physiologic uptake and other Tumour bulk
patterns of diseases with increased FDG uptake indicates lymphoma, The extent of mediastinal disease had been defined based on the ratio
regardless of their size. For patients who have undergone CT scan between the maximum single width of the mediastinal mass on a
898 Revised staging system for malignant lymphoma

standing Posterior-Anterior view (PA) chest X-ray and the maximum patients with FDG-avid lymphoma is assessed using FDG-PET/CT as
intrathoracic diameter on the same radiograph. A ratio greater than the FDG-PET/CT scan frequently demonstrates more sites of bone
or equal to 1/3 was defined as a bulky mass, and the presence of involvement than the CT scan.
a bulky mass was designated by subscript letter ‘X’ in the previous
staging system. In the Lugano classification, a single nodal mass of
10 cm or greater than a third of the transthoracic diameter at any Spleen involvement
level of thoracic vertebrae as determined by a CT scan was defined as In the previous classification, spleen involvement has been sug-
bulky disease for only HL. A chest X-ray is not required to determine gested by unequivocal palpable splenomegaly and confirmed by
tumour bulk because of its high concordance with CT scan. On the the ultrasound or CT scan. In Lugano classification, FDG-PET/CT
contrary, none of the proposed sizes have been validated for NHL in is considered to be the best imaging technique to confirm splenic
the rituximab era. Therefore, the recommendation for NHL and HL involvement in patients with lymphoma. Positive findings on FDG-
is to record the longest measurement by CT scan, with the term ‘X’ PET/CT include diffuse uptake, a solitary mass, miliary lesions or
no longer used in the Lugano classification. nodules, and those on CT scan include enlargement of >13 cm in
cranial-caudal dimension, a mass or nodules that are neither cystic

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nor vascular.
Disease-related symptoms (A and B classifications)
The Ann Arbor classification was used to divide patients according
to absence (A) or presence (B) of disease-related symptoms [fever Liver involvement
(unexplained fever with temperature >38◦ C), night sweats (drench- Liver involvement has been demonstrated by presence of multi-
ing sweats) and weight loss (unexplained weight loss of >10% of the ple focal defects that are neither cystic nor vascular, based on
usual body weight within 6 months prior to diagnosis)]. However, the imaging studies. In Lugano classification, similar to splenic
these clinical features are frequently neither recorded nor accurate, involvement, FDG-PET/CT is recommended for the evaluation of
and these symptoms do not appear to correlate with the outcome in liver involvement by lymphoma and diffusely increased or focal
any of the commonly used prognostic factors in NHL. Thus, these uptake, with or without focal or disseminated nodules, supports liver
symptoms do not need to be applied to NHL as they do not impact involvement.
the management of NHL. In NHL, clinicians are recommended
to record the presence of disease-related symptoms. By contrast,
patients with HL need to be assigned the designations A or B in CNS involvement
the Lugano classification as determining the absence or presence With regard to the evaluation of CNS involvement, there are no
of these symptoms is important to decide the appropriate treat- differences between the previous and current classification. CNS
ment strategy for patients with HL, especially those with early-stage involvement is often symptomatic and is demonstrated by (a) a spinal
disease. intradural deposit or spinal cord or meningeal involvement and (b)
parenchymal brain disease. Spinal intradural deposit or spinal cord or
meningeal involvement may be diagnosed on the basis of the clinical
Bone marrow involvement history and findings supported by cerebrospinal fluid examination
The standard evaluation of bone marrow involvement is based with flow cytometry, CT, and/or magnetic resonance imaging (MRI).
on an aspiration and bone marrow biopsy in combination with Parenchymal brain disease can be detected on CT and/or MRI and
immunohistochemistry and flow cytometry. There are no differ- may be confirmed by biopsy.
ences between the previous and current classification. However,
in the Lugano classification, the role of FDG-PET/CT to assess
the bone marrow involvement in patients with HL and DLBCL is Discussion
added.
In HL, bone marrow involvement rarely occurs in the absence In this review, we have highlighted the revised points of staging
of an FDG-avid bone site. Therefore, if FDG-PET/CT is performed system for malignant lymphoma based on the Lugano classification.
as part of the staging evaluation, routine bone marrow aspiration The most important change was that FDG-PET/CT became the
and biopsy are no longer required for staging of HL. In DLBCL, new standard imaging study for staging of all FDG-avid histologies.
FDG-PET/CT is more sensitive than bone marrow biopsy but has Due to the introduction of FDG-PET/CT for staging, the evaluation
been reported to miss low-volume diffuse involvement. Therefore, of not only lymph node involvement but also organ involvement,
although the presence of FDG-avid skeletal lesions precludes the including liver or spleen, has become simplified. Furthermore, it
need for a bone marrow aspiration and biopsy, bone marrow biopsy could eliminate bone marrow biopsies in patients with HL and
generally should be done in the absence of FDG-avid bone disease to most of the DLBCL. However, delaying the initiation of treatment
identify discordant bone marrow involvement by a low-grade B-cell until the end of FDG-PET/CT is not recommended especially for
lymphoma if relevant for a clinical trial or patient management. In aggressive lymphoma including DLBCL. Furthermore, FDG-PET/CT
addition, as the data in all other histologies are insufficient to change is not the perfect modality for evaluation of lesions. For example,
the standard practice, bone marrow aspiration and biopsy remain the many types of histologies including DLBCL, FL and mantle cell lym-
standard evaluation tool. phoma (MCL) present gastrointestinal lesions. In order to detect the
presence of these gastrointestinal lesions, esophagogastroduodenal
endoscopy (EGD) is preferred and is considered as a conventional
Bone involvement staging method. Furthermore, in patients with MCL, colonoscopy is
In the previous classification, appropriate imaging studies and a also preferred as initial staging procedure, because MCL frequently
biopsy of an involved area of bone were recommended to confirm infiltrate intestinal tract. A retrospective analysis was conducted to
bone involvement. In the Lugano classification, bone involvement in assess the concordance between FDG-PET/CT based on the clinical
Jpn J Clin Oncol, 2019, Vol. 49, No. 10 899

stage and the conventional evaluation including CT scan and EGD in lymphoma. These criteria should be well understood in order to
patients with DLBCL. Results showed that FDG-PET/CT has a low select the appropriate treatment and provide the correct prognostic
sensitivity for the detection of gastrointestinal lesions (12). However, classification. Along with the rapid development of imaging tech-
based on a small retrospective analysis, even in FDG-PET/CT staging nologies, continuous discussions and revisions of these criteria are
era, EGD may be recommended as the routine staging procedures for needed in order to build up the more clinically relevant staging system
FDG-avid histologies, mainly for DLBCL. These data suggested that and select the appropriate management for patients diagnosed with
FDG-PET/CT cannot completely replace the conventional evaluation malignant lymphoma.
tool for staging of malignant lymphoma.
As mentioned above, Ann Arbor classification was originally
intended for HL; that is to say, for evaluation of nodal lesions, the Funding
results of staging evaluation in patients having extranodal lesions This work was supported in part by the National Cancer Center
may differ depending on the physician. For example, stage IIE Research and Development Funds (29-A-3) and AMED under grant
or stage IV might be difficult to assess in patients with a nodal number 18ck0106220h0003.
lesion close to an extranodal lesion. However, as the indication for

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radiotherapy is limited to only patients with possible advanced stage
disease, we believe that the influence this staging inconsistency on Conflict of interest statement
treatment strategies is not significant. In addition, staging system
None declared.
based on both Ann Arbor classification and Lugano classification
cannot cover all patients with malignant lymphoma. For paediatric
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