Dr Cynthia (Jurnal) Clinical Utility of PETCT in Lymphoma
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Transcript of Dr Cynthia (Jurnal) Clinical Utility of PETCT in Lymphoma
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8/16/2019 Dr Cynthia (Jurnal) Clinical Utility of PETCT in Lymphoma
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AJR:19 4, January 2010 W91
ing role. Optimal management of lymphoma
requires that the interpreting radiologist be
familiar with the role of PET/CT in base-
line staging and assessment of therapeutic
response, be aware of the imaging pitfalls
that may be encountered, and understand the
natural behavior of lymphoma and the thera-
peutic options available. The most effective
use of PET/CT therefore requires multidis-
ciplinary collaboration between radiologist,
clinical oncologist, and radiation oncologist.
Overview of Classification of
Lymphoproliferative Disorders
The lymphoproliferative disorders en-
compass a collection of lymphoid neoplasms
with different clinical and histologic presen-
tations. These malignant diseases are linked
by origin within the lymphoid system and
its various cellular components. Hodgkin’s
lymphoma is separated from other lympho-
mas by the light microscopic identificationof Reed-Sternberg cells within the tumor tis-
sue. Non-Hodgkin’s lymphoma accounts for
approximately 2.6% of all cancer deaths, and
the incidence is increasing annually, largely
because of the increasing size of the elder-
ly population, greater accuracy in diagnosis,
the HIV epidemic, and unknown environ-
mental factors. Interestingly, this increasing
incidence has not been reported for Hodg-
kin’s lymphoma, which has a steady annual
Clinical Utility of PET/CTin Lymphoma
Carmel G. Cronin1
Ronan Swords2
Mylene T. Truong3
Chitra Viswanathan3
Eric Rohren3
Francis J. Giles2
Michael O’Dwyer4
John F. Bruzzi1
Cronin CG, Swords R, Truong MT, et al.
1Department of Radiology, University College Hospital
Galway, Galway University Hospitals, Newcastle Rd.,
Galway, Ireland. Address correspondence to C. G. Cronin.
2Division of Hematology and Medical Oncology, Cancer
Therapy and Research Center, Institute for Drug
Development, University of Texas Health Science Center,
San Antonio, TX.
3Department of Diagnostic Imaging, M. D. Anderson
Cancer Center, Houston, TX
4Department of Hematology, University College Hospital
Galway, Galway University Hospitals, Galway, Ireland.
Nuclear Medic ine and Molecular Imaging • Review
WEB
This is a Web exclusive article.
AJR 2010; 194:W91–W103
0361–803X/10/1941–W91
© American Roentgen Ray Society
The lymphoproliferative disorders,
broadly divided into Hodgkin’s
and non-Hodgkin’s lymphoma,
as a group account for one of the
most common malignant diseases in the gen-
eral population. The estimated incidence of
lymphoma in the United States for 2008 was
74,340 cases (66,120 new cases of non-Hodg-
kin’s and 8,220 cases of Hodgkin’s lympho-
ma) and 20,150 deaths [1]. Although the an-
nual incidence of non-Hodgkin’s lymphoma
appears to be slowly increasing, the 5-year
survival rate has been steadily improving in
conjunction with constant refinements in
clinical management aimed at achieving the
highest remission rates with the lowest risk of
therapy-related complications.
Imaging traditionally has played an inte-
gral role in the initial staging and surveil-
lance of lymphoma, primarily through the
use of CT for detection of sites of disease
and monitoring of morphologic changes af-ter treatment. The relatively recent integra-
tion of PET/CT into routine oncologic im-
aging has further improved baseline staging
and facilitated functional evaluation of dis-
ease behavior, metabolic response to therapy,
and earlier detection of disease recurrence.
Consensus guidelines [2, 3] have been pub-
lished that set out updated response criteria
for evaluation of tumor response to thera-
py, and PET/CT is assigned a central imag-
Keywords: lymphoma, PET/CT
DOI:10.2214/AJR.09.2637
Received February 22, 200 9; accepted after revision
July 6, 2009.
OBJECTIVE. The purpose of this review is to assist interpret ing radiologists in becoming
familiar with the role of PET/CT in baseline staging and therapeutic response assessment in
the management of lymphoma, in becoming aware of imaging pitfalls, and in understanding
the natural behavior of lymphoma and the therapeutic options.
CONCLUSION. Therapeutic strategies for the management of lymphoma are constant-
ly being refined to improve long-term survival with the lowest risk of toxicity to the patient.
PET/CT is accurate for baseline staging and yields important prognostic information for de-termining the most appropriate initial treatment. Used for evaluation of treatment response,
PET/CT can depict residual viable malignant lesions with greater accuracy than can other
imaging techniques. The findings thereby influence decisions about the need for additional
or alternative treatment.
Cronin et al.PET/CT of Lymphoma
Nuclear Medicine and Molecular ImagingReview
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incidence of approximately three cases per
100,000 persons.
The classification of lymphoid malignant
diseases has been beset by difficulties. Initial-
ly, the existence of several classification sys-
tems resulted in confusion and difficulty in
comparing the results of clinical trials. With
increasing knowledge of immunophenotyp-ing, cell biology, molecular genetics, and the
recognition of new lymphoma entities, a cen-
sus for universal lymphoma classification
came in 1994 in the form of the revised Eu-
ropean-American classification of lymphoid
neoplasms [4]. In the current World Health
Organization system, which was derived
from the revised European-American clas-
sification, non-Hodgkin’s lymphoma is cat-
egorized into more than 20 subtypes on the
basis of cell of origin (B- or T-cell precur-
sor) and morphologic and immunophenotyp-
ic data [5]. Diffuse large B-cell lymphoma
and follicular lymphoma account for more
than 50% of cases of non-Hodgkin’s lym-
phoma. The clinical behavior of lymphomas
informs management strategies in clinical
practice. Systems in which non-Hodgkin’s
lymphoma is grouped into indolent, aggres-
sive, and very aggressive disorders are prac-
tically very useful. Classification systems are
not static, and it is inevitable that the current
World Health Organization model will be su-
perseded by other systems as more is learned
about the biologic and genetic characteristics
of these disorders.
Diagnosis
As a rule, no specific surface markers are
diagnostic of malignancy of lymphocytes,
and diagnosis is based on an integration of
morphologic (lymph nodes, blood and bone
marrow), immunophenotyping, and molecu-
lar and cytogenetic data. Many lymphomas
have characteristic morphologic features. Ex-
cisional biopsy is preferable over core biop-
sy and fine-needle aspiration for acquisition
of information on structural detail of diagnos-
tic value. In the absence of clinically palpable
lymphadenopathy, suitable sites of biopsy can
be localized with CT or PET/CT. PET/CT hasthe advantage over CT of depicting sites of
lymphoma that are both accessible and meta-
bolically active and therefore most likely to
yield a true-positive result [6].
Several lymphoid neoplasms have unique
antigenic expression on the cell surface that
can be identified with flow cytometry. The
presence of certain antigens, such as CD5,
CD10, and CD23, is helpful in differentiating
clonal B-cell tumors, such as follicular lym-
phoma (CD10+, CD5–, CD23+), from mantle
cell lymphoma (CD10–, CD5+, CD23–). The
immunophenotyping of T-cell neoplasms is
less conclusive than that of B-cell neoplasms
because the former lack the equivalent of
light-chain restriction. Chromosomal trans-
locations in lymphoma often provide diag-
nostic and prognostic information and can
serve as useful response variables over the
course of treatment. Specific translocations,
such as t(14;18) in follicular lymphoma and
t(11;14) in mantle cell lymphoma, often are
sought for these reasons [7].
Staging Systems and Prognosis
Assessment
Staging procedures define the anatom-ic extent of disease and influence choice of
therapy. The Ann Arbor system (Table 1)
was initially devised for use in Hodgkin’s
lymphoma but was later adapted for use in
non-Hodgkin’s lymphoma. Staging is based
on the number and location of nodal stations
involved and the presence or absence of ex-
tranodal lymphoma.
Assessment of prognosis is important for
formulating management strategies. The In-
ternational Prognostic Index (Table 2) is the
most widely used prognostic index for adult
non-Hodgkin’s lymphoma. This index is
based on both clinical and imaging findings
at baseline. The following five factors are
used to predict clinical outcome: age, stage
(modified Ann Arbor), serum lactate dehy-
drogenase (LDH) level, number of extrano-
dal sites of disease, and performance status.
The International Prognostic Index score is
derived from an additive score of 0 to 5 to
stratify patients as having low, intermediate,
or high prognostic risk [8]. Variations of theInternational Prognostic Index are adjusted
for age and presence of follicular lymphoma.
In patients with Hodgkin’s lymphoma,
seven clinical parameters influence outcome
(Table 3). In patients with advanced disease,
TABLE 1: Modif ied Ann Arbor Staging System for Hodgkin’s andNon-Hodgkin’s Lymphoma
Stage Area of Involvement
I Single lymph node region
IE Single extranodal organ or site
II Two or more lymph node regions on the same side of the diaphragm
IIE Localized extranodal extension in addition to criteria for stage II
III Lymph node regions on both sides of the diaphragm
IIIE Localized extralymphatic extension in addition to criteria for stage III
IIIS Splenic involvement (S) in addition to criteria for stage III
IV Dissemination to one or more extralymphatic organs with or without associated lymph nodeinvolvement; involved organs designated by subscript letters (P, lung; H, liver; M, bonemarrow); A used to indicate asymptomatic and B, symptomatic; unexplained fever≥ 38°C;unexplained drenching night sweats; loss of > 10% body weight within previous 6 mo
TABLE 2: International Prognostic Index
Prognosis 0 Points 1 Point Point Total
Parameter
Age < 60 y ≥ 60 y
Modified Ann Arbor stage I, II III, IV
Serum lactate dehydrogenase level Normal Elevated
Extranodal involvement 0–1 site > 1 site
Performance status 0–1 2–4
Risk category
Low 0–1
Low–intermediate 2
Intermediate–high 3
High 4–5
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scores of 0–2 are predictive of a 75% chance
of having no progression of disease 5 years af-
ter diagnosis compared with 55% for scores of
3 or higher [9]. Treatment decisions are based
on several parameters, of which the histologic
features of the tumor, baseline prognostic in-
dicators [9], and stage of disease are of criti-
cal importance.
PET/CT in Initial Staging:
Indications and Utility
CT is the most readily available and most
commonly used tool for staging lymphoma.Fundamental l imitations of CT, however, are
that recognition of lymph node involvement
in disease is based solely on size and that de-
tection of bone marrow and extranodal tissue
involvement may be limited. In addition to de-
picting nodal sites of lymphoma with greater
accuracy than CT, PET/CT has greater sensi-
tivity for sites of extranodal involvement and
correspondingly has been found to improve
baseline staging compared with conventional
staging with CT alone [10, 11] (Figs. 1 and 2).
PET/CT findings also can indicate the over-
all level of metabolic activity of lymphoma,
which correlates with level of aggressivenessand with LDH level (a prognostic predictor).
In general, indolent follicular lymphoma is
associated with low-grade FDG uptake and a
low LDH level, whereas higher intensities of
FDG uptake are seen in more aggressive lym-
phoma with higher LDH levels [12].
Systematic staging of lymphoma by the
radiologist should include the following:
description of nodal stations involved; rep-
resentative unilinear measurements of en-
larged lymph nodes in the long axis; iden-
tification of sites of extranodal involvement;
and detection of coexisting abnormalities
that can affect management, such as infec-
tion in the lungs and facial sinuses and inci-
dental pathologic and malignant changes [2,
3, 9–12] (Fig. 3).
A number of imaging findings are specif-
ically associated with poor prognosis. The
number and location of nodal stations in-
volved by lymphoma adversely affect prog-
nosis and influence the immediate and subse-quent management strategies (Figs. 1, 2, and
4). The presence of bulky disease (any lymph
node mass larger than 10 cm in diameter or an
intrathoracic mass larger than one third the di-
ameter of the thorax) is a poor prognostic in-
dicator and often mandates involved-field ra-
diotherapy after combination chemotherapy.
The presence of extranodal lymphoma also is
a poor prognostic indicator (signifying stage
IV disease) and generally mandates systemic
rather than local treatment. Extranodal sites
of lymphoma include the bone marrow, liver,
lungs, pleura, and other nonlymphoid organs
(Figs. 2 and 5). It is important to differentiatelymphoma originating in an extranodal loca-
tion and thus stage III or IV (e.g., bone mar-
row, liver, or node involvement of the lungs)
from involvement of an extranodal location by
direct extension from a contiguous site of nod-
al disease. Extranodal involvement due to di-
rect extension does not directly influence nodal
stage, and disease remains stage I or II de-
pending on whether lymph nodes are involved
above or below the diaphragm, but the nodal
stage is assigned an E denominator to signify
that disease has spread from lymph nodes to
adjacent extranodal tissue. This differentiation
can be difficult and usually is determined by
the location of the epicenter of disease.
Low-Grade Lymphoma
Low-grade lymphoproliferative disorders
include both B-cell (e.g., chronic lymphocytic
leukemia, follicular lymphoma, marginal zone
lymphoma, and small lymphocytic lymphoma)
and T-cell (peripheral T-cell lymphoma) disor-ders. In general, these disorders progress slow-
ly and are considered incurable. Treatment is
directed at control of symptoms (fatigue, dis-
figuring lymphadenopathy) when they become
clinically important. These lesions typically
have low metabolic activity and have only
low-grade or no FDG uptake. The qualitative
appearance on PET images can be variable,
however, showing a large degree of overlap
Fig. 1—44-year-old man with follicular lymphoma andpalpable left axillary lymphadenopathy. After clinicalexamination and initial CT, patient was believed tohave stage II disease. Additional staging with PET/CT was performed. Coronal maximum-intensity-projection PET image shows enlarged FDG-avidlymph nodes (arrowhead ) in left axilla. Additionalfocus of abnormal FDG uptake (arrow ) is present inleft inguinal region. Because of this finding, diseaseseverity was increased to stage III (involvement oflymph nodes above and below diaphragm).
TABLE 3: Factors Adversely Influencing Outcome of Hodgkin’s Lymphoma
Factor Value
Early stage disease (I–IIIA)
Age > 50 y
Ery throcyte sedimentat ion rate > 50 mm/h
> 30 mm/h with B symptoms (fever, night sweats, weightloss > 10%)
No. of separate nodal sites involved ≥ 4
Mediastinal mass > 10 cm
Advanced stage disease (IIIB–IV)
Age > 45 years
Sex Male
Stage IV
Hemoglobin concentration < 10.5 g/dL
Albumin concentration < 40 g/L
Lymphocyte count < 0.6 × 109 /L or < 8%
WBC count > 15 × 109 /L
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with more aggressive extranodal marginal
zone lymphoma [13, 14].
Because the stage of the disease is less im-
portant than the clinical manifestations, PET/
CT is not used for routine staging. In certain
instances, however, PET/CT can be useful in
the management of low-grade lymphoma. Pa-
tients with low-grade, aggressive, or highly
aggressive lymphoma in the early stage or lo-
calized (stage I or II, comprising involvement
of a single lymph node station or two lymph
node stations on one side of the diaphragm,
respectively) without bulky disease can be
treated with curative intent with involved-
field radiotherapy with or without an abbrevi-ated course of chemotherapy [15, 16]. In the
care of such patients, PET/CT is important for
excluding unexpected sites of nodal or extra-
nodal lymphoma [17] (Figs. 1 and 4), which
would necessitate prolonged chemotherapy
(six to eight cycles). Radiotherapy would be
reserved for bulky disease. PET/CT also can
be useful for baseline assessment of patients
with refractory disease undergoing new lines
of treatment. It thereby facilitates assessment
of response to therapy (see later, Assessmentof Therapeutic Response).
In a small percentage of patients, trans-
formation of indolent lymphoma to a higher
grade of lymphoma can occur, most common-
ly in diffuse large B-cell lymphoma (known
as Richter’s transformation). Lymphomatous
transformation is associated with a very poor
prognosis and is an indication for high-dose
chemoimmunotherapy and postremission stem
cell transplantation [18]. Transformation is sus-
pected in patients with rapidly enlarging lymph
nodes, an increasing LDH level, or new onset of
B symptoms (fever, night sweats, and weight
loss greater than 10%). In the care of such pa-
tients, PET/CT has been found to be of value
in detecting transformation by depicting ab-
normally elevated FDG uptake at sites of trans-
formation (indolent lymphoma normally has
only low-grade FDG uptake) [18, 19] (Fig. 6).
Sites of suspected transformation should be
biopsied for confirmation of the diagnosis.
Aggressive and Highly Aggressive
Lymphoma
Aggressive and highly aggressive non-Hodg-
kin’s lymphomas, of which diffuse large B-cell
lymphoma is the most common, generally ex-hibit marked elevation in FDG uptake at PET/
CT. Compared with conventional staging with
CT alone, staging with PET/CT can lead to an
BA
Fig. 2—20-year-old man with recently diagnosedBurkitt’s lymphoma. Example of PET/CT patterns ofextranodal involvement by lymphoma and baselinestaging with PET/CT.A and B, Coronal (A) and axial (B) fused PET/CTimages show extent of disease involvement, intenseFDG uptake being evident within retroperitoneallymphadenopathy (arrowhead, A). Activity withinliver (short arrow, B) and peritoneum (long arrows )
indicates extranodal lymphoma, representing stageIV disease. Diffuse bone marrow involvement alsois present. Extranodal involvement of bones, liver(short arrow, B), and peritoneum (long arrows ) wasindeterminate or occult on conventional contrast-enhanced CT images, and stage IV disease was notdiagnosed prospectively.
A CB
Fig. 3—53-year-old man with stage III diffuse large B-cell lymphoma.A, Coronal maximum-intensity-projection PET image from baseline staging PET/CT scan shows FDG-avidlymphadenopathy above and below diaphragm. Focus of increased FDG uptake in left side of pelvis (arrow ) waspresumed to represent additional site of lymphoma.B and C, Axial fused PET/CT (B) and contrast-enhanced diagnostic CT (C) images show abnormal activity(arrow ) in segment of thick-walled sigmoid colon. Colonoscopy confirmed area represents incidental coloniccarcinoma, not residual lymphoma.
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increase in stage because active lymphoma
can be depicted in subcentimeter lymph nodes;
unexpected extranodal sites of disease and vis-
ceral involvement of liver and spleen also can
be depicted [20–22] (Figs. 1, 2, and 4).
Although a baseline PET/CT examina-
tion is strongly advised in the care of all pa-
tients with aggressive or highly aggressive
non-Hodgkin’s lymphoma for refining initialstaging and prognosis assessment, it is not al-
ways strictly necessary. For example, when
the initial stage is clear from conventional
imaging findings (e.g., unequivocal stage IV
disease) or the initial treatment plan incorpo-
rates a full course of chemotherapy, baseline
PET/CT findings are unlikely to change the
management decision [2, 3].
Patients with poor baseline prognostic in-
dicators are at risk of having disease refrac-
tory to treatment or of having a relapse soon
after completing therapy. These patients may
be candidates for stem cell transplantation im-
mediately or at first relapse. In such instances,
posttherapy PET/CT findings may be difficult
to interpret without baseline PET/CT images
for comparison, particularly if residual areas
of abnormal FDG uptake are present (see later,
Assessment of Therapeutic Response) [2, 3].
Hodgkin’s Lymphoma
Although Hodgkin’s lymphoma is staged
the same way as non-Hodgkin’s lymphoma
(modified Ann-Arbor classification), it dif-
fers from non-Hodgkin’s lymphoma in its
propensity to spread by contiguous nodal in-
volvement rather than multifocal nodal in-
volvement. Nodular sclerosing Hodgkin’s
lymphoma, the most common histologic type,
usually manifests itself as lymphadenopathy
above the diaphragm; isolated infradiaphrag-
matic lymph node involvement is rare. Hodg-kin’s lymphoma is FDG avid, and PET/CT is
a more accurate initial staging examination
than conventional diagnostic CT [20], par-
ticularly for detection of unexpected sites of
extranodal lymphoma.
In clinical practice, assessment of progno-
sis determines the role of PET/CT in base-
line staging and response assessment. For
example, for patients with a good prognostic
index at baseline and eminently curable lym-
phoma (e.g., diffuse large B-cell lymphoma
or Hodgkin’s lymphoma), baseline PET/CT
is less important than posttreatment PET/
CT, which is used to confirm the success of
treatment and exclude residual viable malig-
nancy (see later, Assessment of Therapeutic
Response). In patients with a poor prognos-
tic index at baseline, it may be appropriate
to perform PET/CT early in the course of
therapy (e.g., after two to four cycles of che-
motherapy) to detect refractory disease, the
presence of which can influence subsequent
treatment decisions.
Imaging Pitfalls
Lymphoma With Variable FDG Uptake
Certain subtypes of lymphoma, such asextranodal marginal zone lymphoma [23]
and T-cell cutaneous lymphoma [24], exhib-
it variable FDG uptake (Fig. 7) and can be
difficult to detect with conventional contrast-
enhanced CT. In such cases, initial baseline
PET/CT is particularly important for facili-
tating assessment of therapeutic response. It
would be difficult to interpret the true clini-
cal meaning of residual abnormal FDG up-
take after therapy if there were no baseline
scan for comparison.
Lymphoma Difficult to Detect With PET/CT
Subtypes of lymphoma difficult or impos-sible to detect with PET/CT include prima-
ry CNS lymphoma, testicular lymphoma,
and gastric lymphoma. Because of the in-
tense physiologic uptake of FDG by normal
cerebral tissue, CNS lymphoma can be diffi-
cult to detect without appropriate adjustment
of the image intensity thresholds. In the case
of testicular lymphoma, for which patients
are normally treated with orchiectomy and
combination chemotherapy, it is impossible
to differentiate FDG uptake by the malignant
tumor from normal physiologic testicular ac-
tivity. It is important to note that on follow-up
PET/CT scans, FDG uptake in the contralat-
eral testis is normal and without further eval-
uation should not be presumed to represent
recurrent testicular lymphoma. Gastric lym-
phoma typically exhibits no FDG uptake or ex-
hibits variable FDG uptake that is difficult or
impossible to differentiate from normal activi-
ty in the gastric mucosa. These patients may be
candidates for radiation therapy only, particu-
larly in cases of gastric mucosa–associated
A
Fig. 4—63-year-old woman with follicular lymphomanewly diagnosed after biopsy of retroperitonealmass. Baseline staging with PET/CT.A, Coronal CT image shows large retroperitonealmass consistent with known site of biopsy-proven lymphoma (arrowhead ). Also present areindeterminate subcentimeter lymph nodes in axillae(long arrows ). Spleen (short arrow ) is of normal size.At CT, mass was considered stage II, represent ing
involvement of more than one lymph node station onone side of diaphragm.B, Coronal fused PET/CT image shows intense FDGuptake by retroperitoneal mass (arrowhead ) andabnormal FDG uptake in small axillary lymph nodes(long arrows ). Unexpected FDG-avid lymph node (thick short arrow ) was found in left infraclavicular region.Diffuse intermediate-grade FDG uptake in spleen (thin short arrow ) greater than that in liver is considered torepresent diffuse lymphomatous infiltration. Diseaseseverity was increased to stage IIIS.
B
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lymphoid tissue lymphoma or mucosa-related
lymphoid tissue lymphoma, if disease is lim-
ited to the stomach. In these cases the main
purpose of PET/CT is to exclude lymphoma
elsewhere [25–28].
Lymphoma With Particular Patterns
of Spread and Relapse
Certain types of aggressive lymphoma not-
ed for their patterns of spread and relapse re-
quire particular attention. CNS involvement
is relatively common with sporadic Burkitt’s
lymphoma, and interpretation of the baseline
PET/CT images should include examination
of the brain with appropriate threshold set-
tings. Lymphoblastic lymphoma and adult
T-cell lymphoma commonly manifest them-
selves as large mediastinal masses that can
be associated with pericardial involvement.These findings can be difficult to detect with
CT alone. Identification of abnormal peri-
cardial uptake of FDG at PET/CT suggests
the presence of lymphomatous involvement
in these cases [29]. A very high-fat, low-
carbohydrate, protein-permitted meal 3–6
hours before FDG injection has been found
to suppress myocardial FDG uptake and may
be beneficial in these circumstances for de-
picting mediastinal, pericardial, and cardiac
lymphomatous disease [30].
Bone Marrow InvolvementAlthough PET/CT can depict bone mar-
row involvement in patients with negative re-
sults of iliac crest biopsy [31] (Fig. 8), fre-
quent false-positive findings are caused by
diffuse or heterogeneous FDG uptake sec-
ondary to reactive marrow hyperplasia (Fig.
5). In addition, microscopic marrow involve-
A C D EB
Fig. 5—Patterns of bone marrow involvement by lymphoma.A and B, 24-year-old woman with Hodgkin’s lymphoma. Sagit tal fused PET/CT image (A) shows multiple foci of intense FDG uptake (arrows ). Sagittal T1-weighted MRimage (B) shows multifocal pattern of bone marrow involvement (arrows ). CT-guided biopsy of L3 lesion confirmed marrow involvement by Hodgkin’s lymphoma (stage IV) .C and D, 56-year-old man with mantle cell lymphoma (stage IV). Coronal (C) and sagittal (D) PET images show diffuse patchy heterogeneous pattern of FDG uptake. Bonemarrow biopsy result was positive for lymphoma.E, 64-year-old man treated for non-Hodgkin’s lymphoma. Sagittal PET image shows diffuse homogeneous pattern of FDG uptake within bone marrow of vertebralbodies caused by bone marrow hyperplasia secondary to cytokine administration. In absence of adequate clinical information, it is often impossible to differentiate thisappearance from diffuse lymphomatous infiltration of bone marrow (C and D).
A
Fig. 6—57-year-old man with long-standing smalllymphocytic lymphoma and suspected Richter’s
transformation.A, Axial fused PET/CT image from baseline PET/CT examination shows extensive intraabdominallymphadenopathy (arrowhead ) associated with
diffuse low-grade or intermediate-grade FDGuptake consistent with low-grade small lymphocyticlymphoma. More-marked FDG uptake is present inlymphadenopathy (arrow ) in left side of pelvis. Finding issuspicious for transformation to high-grade lymphoma,which was subsequently confirmed with biopsy.B, Axial fused PET/CT image obtained for restagingafter chemotherapy shows almost completeresolution of metabolic activity in transformedhigh-grade lymphoma (arrow ) in pelvis butpersistent activity in low-grade small lymphocyticlymphoma (arrowhead ), which is more resistant tochemotherapy.
B
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ment can be below the limits of detection
with PET/CT, accounting for the relatively
low sensitivity of this technique in the detec-
tion of bone marrow lymphoma (≈ 43% for
non-Hodgkin’s lymphoma) [32]. For these
reasons, bone marrow biopsy remains the
reference standard for assessment of bone
marrow. However, focal areas of intense
FDG uptake in the bone marrow remain sus-
picious for lymphoma even when the findings
at iliac crest biopsy are negative and should
be further evaluated with targeted biopsy or
MRI (Fig. 5).
Assessment of Therapeutic Response
Imaging evaluation of therapeutic re-
sponse once was limited to monitoring of
changes in lymph node size with CT. The
residual lymph node mass was a common-
ly encountered diagnostic challenge because
it is difficult at CT to differentiate posttreat-
ment fibrosis from residual viable malig-
nant changes. PET/CT has been found use-
ful in assessment of therapeutic response
because of its improved utility in discrimi-
nating benign fibrosis (low-grade or absent
FDG uptake) and residual active lymphoma
(elevated FDG uptake). PET/CT cannot be
used, however, to exclude microscopic ma-
lignant change below its threshold of detect-
ability. In 2007, the International Harmo-
nization Project was convened to revise the
older CT-based response criteria [2, 3]. The
A B
Fig. 7—53-year-old man with progressive blasticnatural killer cell cutaneous T-cell lymphoma of upperback. Baseline staging PET/CT showed FDG-avidcutaneous nodule but no disease elsewhere (notshown). Restaging PET/CT was performed becauseof progressive enlargement of cutaneous mass.A, Axial PET/CT image shows marked FDG uptake bylarge cutaneous soft-tissue mass in upper back.B, Coronal fused PET/CT image shows diffuse FDG
uptake within enlarged spleen (arrowhead ) andpatchy uptake in bone marrow (arrows ) consistentwith stage IV lymphoma. Patient underwent systemicchemotherapy.
A
Fig. 8—31-year-old man with progressive refractory Hodgkin’s lymphoma and history of tuberculosis undergoing assessment for bone marrow transplantation.A, Axial CT image from PET/CT examination shows area of bone sclerosis (arrow ) adjacent to right sacroiliac joint.B, Axial fused PET/CT image shows no abnormal FDG uptake in area of sclerosis, but abnormal activity (arrow ) is present in left sacral ala. Subsequent biopsy of rightsacroiliac joint showed no evidence of lymphoma but showed acid-fast bacilli. Patient was treated with 2-month regimen of antituberculous therapy.C, Follow-up axial fused PET/CT image shows new area of abnormal FDG uptake (arrow ) in region of sclerosis in lower thoracic spine. Biopsy confirmed recurrentlymphoma. Appearance of bone marrow involvement by lymphoma is variable at CT, and correlation with pattern of FDG uptake and with previous imaging findings isessential to avoiding confusion.
CB
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recommendations emphasize the importance
to the interpreting radiologist of having ad-
equate clinical information available and ofbeing familiar with the limitations and inter-
pretative pitfalls of PET/CT. These new ther-
apeutic response criteria are summarized in
Table 4.
Definition of Positive PET/CT Findings
After Treatment
Because of variability among patients,
scans, and observers in calculation of semi-
quantitative measurements of FDG activity,
such as maximum standardized uptake val-
ue, visual analysis is sufficient for assessment
of therapeutic response. Any lymph node
smaller than 2 cm in diameter with FDG up-
take greater than the uptake in surrounding
background tissue is considered positive for
active lymphomatous involvement [2, 3]. For
lymph node masses larger than 2 cm, any ac-
tivity greater than that in mediastinal blood
pool structures is considered positive for
active lymphoma, which allows low-grade
FDG uptake secondary to blood pool activ-
ity after treatment [2, 3].
In the liver and spleen, focal lesions with
activity greater than that in surrounding liv-
er or spleen parenchyma are considered posi-tive for viable lymphoma. Diffuse FDG up-
take by the spleen with an intensity greater
than that in the liver also is considered pos-
itive for lymphoma in the absence of other
confounding factors, such as physiologic hy-
perplasia after cytokine administration [2, 3]
(Fig. 9). The presence of single or multiple
foci of clearly elevated FDG uptake within
the bone marrow also is considered positive
for active lymphoma [2, 3] (Fig. 5). In cases
in which vertebral body involvement is sus-
pected, the CT images should be carefully
examined for signs of spinal canal encroach-
ment that warrant radiotherapy.
Utility of PET/CT for Assessment
of Treatment Response
The objective of posttreatment PET/CT
depends on the clinical situation and the tim-
ing of the examination (during or after com-
pletion of therapy). In most instances PET/
CT is performed after completion of treat-
ment, in which case the primary purpose is to
detect residual active lymphoma (i.e., to con-
firm or exclude complete remission according
to the response criteria). Persistent disease isassociated with early relapse and poor clini-
cal outcome, and further therapy may be in-
dicated [33, 34]. Studies [35, 36] have shown
the prognostic value of PET/CT during and
after chemotherapy for identifying cases in
which the patient needs further, intensified
treatment. PET/CT occasionally is performed
earlier in the course of treatment (after two to
four cycles of a six- to eight-cycle regimen),
when evidence of refractory disease may lead
to changes in treatment regimens [37] (Fig.
10). Convincing evidence shows that persis-
tent FDG uptake after two to four cycles of
chemotherapy is associated with poor clini-
cal outcome [38–41]. It has not yet been con-
clusively proven, however, that changing che-
motherapeutic regimens midway through
treatment on the basis of PET/CT findings
improves outcome [42].
Low-Grade Lymphoma
In patients with indolent or otherwise in-
curable lymphoma (e.g., chronic lymphocytic
TABLE 4: International Harmonization Project Criteria for Assessment of Response to Therapy for Lymphoma
Response FDG-Avid at Baseline Not FDG-Avid at Baseline
Complete remission Complete resolution of FDG-avid lesions and negative result of bone marrowbiopsy
Return to normal size of lymphadenopathy withcomplete resolution of ex tranodal disease
Partial remission > 50% decrease in sum or product of diameters of lesions with persistentresidual FDG uptake in at least one site
> 50% decrease in sum or product of diameters oflesions
Progressive disease Any new FDG-avid lesion; ≥ 50% increase in sum or product of diameters ofpreviously involved sites with respect to nadir sum or product of diametersassociated with abnormal FDG uptake; or new or recurrent bone marrowinvolvement
Any new lesion > 1.5 cm in any axis; ≥ 50% increase insum or product of diameters of previously involvedsites with respect to nadir sum or product ofdiameters; or new or recurrent bone marrowinvolvement
Stable disease No complete remission, partial remission, or progressive disease No complete remission, partial remission, orprogressive disease
Note—Summarized from [2].
A
Fig. 9—Patterns of splenic involvement bylymphoma.A, 66-year-old man with relapsed diffuse large B-celllymphoma. Axial fused PET/CT image shows multiplehypodense masses (arrows ) in enlarged spleen thatare FDG avid.B, 68-year-old woman with relapsed diffuse large
B-cell lymphoma. Axial PET/CT image showsdiffuse FDG uptake (arrow ) greater than that in liver.Finding is consistent with diffuse lymphomatousinvolvement.
B
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leukemia, small lymphocytic lymphoma,
and marginal zone lymphoma), therapeutic
response generally is measured in terms of
symptom relief, progression- and event-freesurvival, and overall survival.
Aggressive and Highly Aggressive
Non-Hodgkin’s Lymphoma
In patients with potentially curable non-
Hodgkin’s lymphoma, a complete metabol-
ic response after treatment is a good indi-
cator of long-term disease-free survival. In
these patients, a complete response to treat-
ment is defined as total absence of abnormal
FDG uptake, as defined earlier. Posttherapy
PET/CT findings of complete response are
considered to indicate the disease is in com-plete remission. Further treatment may con-
sist of two cycles of consolidation chemo-
therapy or routine surveillance. In the care
of patients with PET/CT findings of residual
disease, a clinical decision is required that
may involve continuing therapy, switching
therapy, or consideration of stem cell t rans-
plantation (Fig. 11). The International Har-
monization Project consensus guidelines
recommend that restaging PET/CT ideally
be performed 6–8 weeks after completion
of treatment to minimize confounding FDG
uptake secondary to posttreatment inflam-mation. In the care of patients with poten-
tially curable lymphoma in whom refracto-
ry disease will lead to changes in treatment,
particularly patients who have poor prog-
nostic indices at baseline evaluation, it may
not be practical to wait this long. Never-
theless, PET/CT should generally be per-
formed no sooner than 3 weeks after com-
pletion of therapy [3].
A
Fig. 10—66-year-old man with stage IV diffuse largeB-cell lymphoma.A, Axial fused PET/CT image from baseline PET/CTexamination shows FDG-avid lymphadenopathy inparaaortic regions in addition to splenic involvement(arrowhead ).B, Three cycles of systemic chemotherapy resultedin marked anatomic response with almost completeinterval resolution of lymphadenopathy on CT
images. Fused PET/CT image, however, showspersistent abnormal FDG uptake within small residuallymph node in retroperitoneum (arrow ). Finding isconsistent with residual viable lymphoma, whichis associated with higher probability of refractorylymphoma and is indication for extended therapy.
B
A
Fig. 11—67-year-old man with myelodysplastic syndrome and mantle cell lymphoma who underwent reevaluation with PET/CT after chemotherapy.A, Axial unenhanced CT image from PET/CT examination shows persistent lymphadenopathy measuring more than 2 cm in diameter in retroperitoneum ( arrowhead ) andsmall-bowel mesentery (arrow ).B, Axial fused PET/CT image at same level as A shows FDG uptake in retroperitoneal lymphadenopathy (arrowhead ) is no greater than that in surrounding normal tissue,consistent with absence of detectable metabolically active lymphoma. Arrow indicates lymphadenopathy in small-bowel mesentery.C, PET image shows low-grade FDG uptake within lymphadenopathy in small-bowel mesentery (white arrow ), which is greater than that in mediastinum (black arrow ),consistent with persis tent viable lymphoma. Because of this abnormal FDG uptake, complete remission was not achieved, and second-line chemotherapy was initiated.
B C
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Hodgkin’s Lymphoma
Like aggressive and highly aggressive non-Hodgkin’s lymphoma, Hodgkin’s lymphoma
is routinely FDG avid, and the primary pur-
pose of posttreatment PET/CT is to confirm
or exclude complete remission, that is, the
presence or absence of residual viable ma-
lignancy. PET has consistently been found to
have a high negative predictive value (≈ 90%)
and a somewhat lower positive predictive val-
ue (≈ 65%, lower than in diffuse large B-cell
non-Hodgkin’s lymphoma) in the detection
of viable lymphoma in residual masses af-
ter therapy [33, 34, 36, 43, 44]. The relatively
low positive predictive value is due to postra-
diotherapy inflammation, which can persistas long as 8–12 weeks, and to interobserver
variability in the assessment of posttherapy
FDG uptake. The International Harmoniza-
tion Project guidelines address these issues
for improving the predictive value of PET in
Hodgkin’s lymphoma and to ensure standard-
ization of response assessment.
For early-stage Hodgkin’s lymphoma, sin-
gle-modality radiotherapy is less commonly
used than in the past and usually is combined
with abbreviated chemotherapy (e.g., fourcycles of doxorubicin hydrochloride [Adri-
amycin, Pharmacia] bleomycin, vinblastine,
and dacarbazine). Persistent abnormal FDG
uptake signifies the presence of residual vi-
able lymphoma and is an indication for ex-
tending chemotherapy to a full course. In pa-
tients who have completed six to eight cycles
of standard therapy (with or without the ad-
dition of radiation), persistent FDG uptake
indicates the presence of refractory disease
and is associated with poor long-term sur-
vival. These patients may proceed to high-
dose chemotherapy and autologous stem cell
transplantation, but salvage radiotherapy forlocalized residual disease is still an option in
selected cases.
Pitfalls in Interpretation of
Posttreatment PET/CT Findings
The most frequent difficulties encountered
in interpretation of posttreatment PET/CT
scans include differentiating residual FDG
uptake due to lymphoma from FDG uptake
due to posttreatment inflammation, coexisting
infection, and normal physiologic metabol-ic activity [45–49] (Figs. 5, 8, and 12). Post-
treatment inflammation can persist as long as
2 weeks after completion of chemotherapy
and as long as 3 months after chemoradiation
therapy [2, 3]. Low-grade FDG uptake within
residual lymph node masses should be inter-
preted in light of information about the type
and timing of previous treatment and accord-
ing to the criteria described by the Interna-
tional Harmonization Project. Activity with-
in small lymph nodes (< 2 cm) that is equal to
or less than surrounding background activity
and activity within larger lymph node masses
that is equal to or less than mediastinal bloodpool activity are considered to represent post-
treatment inflammation and not residual vi-
able malignant tissue.
It is useful to be aware of the patient’s cur-
rent treatment, the presence or absence of
neutropenia, and history of infection. Persis-
tent neutropenia increases susceptibility to
opportunistic infections such as fungal pneu-
monia, sinusitis, and typhlitis. Fungal pneu-
A
Fig. 12—56-year-old man with stage IV Burkitt’s lymphoma, which can cause potential false-positive PET/CT findings after chemotherapy.A, Coronal maximum-intensity-projection PET image from baseline staging PET/CT examination shows marked FDG uptake within intraabdominal (mesenteric andretroperitoneal) lymphadenopathy. Patchy bone marrow uptake also is evident.B, Coronal PET image from restaging PET/CT examination after completion of systemic chemotherapy shows interval resolution of abnormal FDG uptake with oneisolated focus of residual abnormal activity in right side of retroperitoneum (arrow ) anterior to psoas muscle. Finding was suspicious for res idual viable lymphoma.C, Axial fused PET/CT image shows abnormal FDG uptake corresponding to physiologic activity within right ureter (arrow ). Appearance represents complete metabolicresponse to therapy.
CB
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monia can manifest itself as ill-defined areas
of consolidation, pulmonary nodules, and
masses and can be associated with abnor-
mal FDG uptake. Differentiation from pul-
monary lymphoma based on the CT appear-
ance alone can be difficult if not interpreted
in the context of the patient’s previous dis-
ease distribution, response to treatment, andhistory of episodes of fungal pneumonia [50,
51]. Previous pneumonia of any cause also
can be associated with low- or intermediate-
grade uptake in draining lymph nodes in the
hila and mediastinum, which can persist for
several weeks after the acute infectious epi-
sode has resolved.
In patients with evidence of previous
granulomatous disease such as tuberculosis
or sarcoidosis, it is common to see low-grade
FDG uptake in hilar and mediastinal lymph
nodes and even in the axillae and abdomen
[52–55]. FDG uptake in the facial sinuses
secondary to active sinusitis or in the colon
secondary to typhlitis or neutropenic colitis
is not easily confused with lymphoma but is
important to note in the interests of imme-
diate management and further immunosup-
pressive treatment [56, 57].
It is important for the interpreting radiolo-
gist to be familiar with other, more generic
causes of FDG uptake due to normal physio-
logic uptake or benign disease [2, 3, 46–48].
Diffuse FDG uptake within the marrow-
containing bony skeleton (vertebral bodies,
proximal long bones, and sternum) may be
physiologic marrow activity secondary to re-bound hyperplasia after chemotherapy or af-
ter cytokine administration (Fig. 5). Bone
marrow biopsy may be required for problem-
solving in selected cases. Physiologic FDG
uptake also can be caused by normal muscle
activity, thymic hyperplasia, brown fat, ath-
erosclerosis, venous thrombosis, and previ-
ous medical and surgical interventions [2, 3].
These common interpretative pitfalls have
been described thoroughly [46, 52, 53, 58].
In all cases, correct PET/CT interpreta-
tion depends on having an adequate knowl-
edge of the clinical history, correlation with
findings of other imaging studies, and famil-iarity with the wide range of potential im-
aging artifacts and interpretative pitfalls that
can be encountered.
Complications of Treatment
In all patients undergoing response assess-
ment with PET/CT, attention should be paid
not only to areas of persistent FDG uptake but
also to signs of possible drug or radiothera-
py toxicity, which can be most evident on the
CT component. Evidence of such toxicity is
important for decisions regarding changes in
treatment regimen, duration of treatment, and
alternative treatments. Treatment-related com-
plications include pulmonary pneumonitis or
fibrosis, which occurs in as many as 18% of
patients receiving bleomycin (part of the Adri-amycin, bleomycin, vinblastine, and dacarba-
zine regimen for Hodgkin’s lymphoma) and
has an associated mortality of 4.2% [59]; car-
diomyopathy secondary to anthracycline (e.g.,
doxorubicin) toxicity, resulting in a 28% in-
creased risk of congestive heart failure [60]; ra-
diation pneumonitis, radiation pericarditis, and
radiation enteritis (less clinically significant in
lymphoma than in the past owing to targeted
3D conformal therapy); and infections second-
ary to neutropenia.
Utility of PET/CT in Stem Cell
Transplantation
In general, patients with aggressive lym-
phoma who have primary refractory disease
or a relapse within a year of achieving com-
plete remission have a poor prognosis. Stem
cell transplantation with autologous or allo-
genic stem cells should be considered in the
care of these patients. The choice of trans-
plantation depends on several factors, in-
cluding the performance status and age of
the patient, the availability of a histocompat-
ible donor, and several other factors that are
beyond the scope of this review.
There is evidence that PET/CT can beused for selection of patients for stem cell
transplantation [56, 57, 59]. In a retrospec-
tive analysis of 60 patients with Hodgkin’s
or non-Hodgkin’s lymphoma scheduled for
high-dose chemotherapy and stem cell trans-
plantation, Spaepen et al. [57] found that per-
sistently abnormal PET findings after salvage
chemotherapy but before stem cell transplan-
tation are predictive of poor progression-free
and overall survival. In a different retrospec-
tive study of patients with Hodgkin’s or non-
Hodgkin’s lymphoma undergoing reinduction
chemotherapy before stem cell transplanta-
tion, Schot et al. [56] found that early PET af-ter two cycles of reinduction therapy can be
combined with a baseline clinical risk score
(secondary age-adjusted International Prog-
nostic Index for recurring non-Hodgkin’s
lymphoma and recurring Hodgkin score for
Hodgkin’s lymphoma) to predict outcome.
Those authors identified four main risk groups
predictive of the rate of success of stem cell
transplantation. They documented success
rates of 80–100% among patients with a low
combined risk score to success rates of 0–7%
among patients with a high combined risk
score. PET/CT therefore may be useful for
selecting patients most likely to respond to
stem cell transplantation, although prospec-
tive data showing changes in treatment based
on PET/CT findings are still lacking.
Conclusion
The lymphoproliferative disorders encom-
pass a wide range of malignant diseases with
differing histologic characteristics, behav-
ior patterns, imaging appearances, and treat-
ment options. Although it is not necessary
for radiologists to have an extensive knowl-
edge of each lymphoma subtype, it is useful
to consider them in terms of a clinicopatho-
logic grading system (indolent, aggressive,
and highly aggressive) that broadly correlates
with management approach and FDG avidi-
ty. PET/CT is most effectively and efficient-
ly used when both the referring clinician and
the radiologist understand the uses and limi-
tations of PET/CT within the context of the
treatment strategy for each patient. Optimal
interpretation of baseline staging and post-
treatment PET/CT scans relies heavily on the
radiologist’s having adequate clinical infor-
mation about the patient, the disease, and the
treatment history. Participation in multidisci-
plinary case conferences is strongly advised.
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