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Blood, Vol. 91 No. 9 (May 1), 1998:
pp. 3340-3346
Detection of Lymphoma in Bone Marrow by Whole-Body Positron
Emission Tomography
By
Robert Carr,
Sally F. Barrington,
Bella Madan,
Michael J. O'Doherty, Catherine A.B. Saunders,
Jon van der Walt, and
Adrian
R. Timothy
From the Departments of Haematology, Histopathology, Clinical
Oncology and The Clinical PET Centre, United Medical and Dental Schools
of Guy's and St Thomas's, London, UK.
 |
ABSTRACT |
Positron emission tomography (PET) is a whole-body imaging technique
using 18 fluorine-fluorodeoxyglucose (FDG), whose uptake is increased
in tumor cells. Published studies have shown PET to be an effective
method of staging lymphoma and to be more sensitive than CT at
detecting extranodal disease. The purpose of this study was to
determine whether the increased marrow uptake of FDG observed in some
lymphoma patients during routine staging PET scans represented marrow
involvement by disease. PET scans of 50 patients with Hodgkin's (12)
and non-Hodgkin's (38) lymphoma were analyzed by three independent observers and the marrow graded as normal or abnormal using a visual
grading system. Unilateral iliac crest marrow aspirates and biopsies
were performed on all patients. The PET scan and marrow histology
agreed in 39 patients (78%), being concordant positive in 13 and
concordant negative in 26 patients. In 8 patients the PET scan showed
increased FDG uptake but staging biopsy was negative; in 4 of these 8 patients the PET scan showed a normal marrow background with focal FDG
"hot spots" distant from the site biopsied. In 3 patients the
marrow biopsy specimen was positive but the PET scan normal; 2 of these
3 patients had non-Hodgkin's lymphoma whose malignant cells did not
take up FDG at lymph node or marrow disease sites. Therefore, there
were only 5 patients (10%) in whom there was a difference between the
PET scan and biopsy result which could not be fully explained. Visual
interpretation of marrow FDG uptake during whole-body staging PET scans
can correctly assess marrow disease status in a high proportion of
lymphoma patients. PET has the potential to reduce the need for staging marrow biopsy.
| |
INTRODUCTION |
BONE MARROW (BM) BIOPSY is an important
part of the routine staging of Hodgkin's disease (HD) and
non-Hodgkin's lymphoma (NHL). BM involvement by lymphoma confers
advanced-stage disease and may affect both treatment and prognosis.
Histological evidence of lymphoma in the BM is found in approximately
50% to 80% of patients with low-grade NHL, 25% to 40% of high-grade
NHL, and 5% to 14% of HD patients at diagnosis.1
The need for a staging marrow biopsy in all cases of lymphoma is the
subject of ongoing debate and has been questioned by some
investigators.2 Studies in NHL have shown that the marrow biopsy findings may not affect management in patients with advanced clinical stages of certain disease subtypes,3 while a
recent United Kingdom survey revealed widely differing practices
amongst hematologists and oncologists in their use of staging biopsy in HD.4 Two factors make the marrow trephine biopsy an
unsatisfactory diagnostic test: it is a painful and invasive procedure
and, even if the volume of the biopsy is adequate, focal lesions can be missed. Several large studies have consistently shown that a unilateral iliac crest trephine biopsy is an unreliable method of detecting marrow
lymphoma, especially in high-grade NHL, where accurate staging is
particularly important. These studies have shown lymphoma to be present
in only one sample of paired bilateral iliac crest trephines in 22% to
30% of NHL cases when all histological grades were included, and this
discrepancy between biopsy sites may occur in as many as 31% to 50%
of high-grade NHLs.5-8 In young patients with lymphoblastic
and large cell lymphoma, disease was present in only one sample in 33%
of paired biopsies, when both were taken from the same iliac
crest.7 Likewise in HD, unilateral marrow disease was found
in 43% of cases.5 Against this background a more reliable,
noninvasive method of detecting lymphoma in the marrow would be
welcome.
Positron emission tomography (PET) is a whole-body imaging technique
that uses positron emitting isotopes of biological elements, such as
carbon, oxygen, nitrogen, and fluorine, for the functional assessment
of perfusion and metabolism in vivo. The most common tracer used in
oncology is the glucose analogue 18 fluorine fluorodeoxyglucose (FDG),
whose uptake is increased into tumor cells, by virtue of their
increased glucose transfer and glycolysis.9,10 Once inside
the cell it is phosphorylated by hexokinase, but is then trapped
because it is effectively unable to enter the subsequent glycolytic
pathways. PET has an advantage over computed tomography (CT) in its ability to detect extranodal disease and to
visualize tumor when there is no anatomical abnormality on
imaging.11,12 The ability of PET to provide high-quality
whole-body images of nodal and extranodal disease at a single scanning
session means that its use is increasing for the primary staging,
remission assessment, and treatment monitoring of
lymphoma.13-17
Studies comparing PET with CT for staging lymphoma have consistently
shown a high degree of concordance in identifying nodal disease and
have shown PET to have greater sensitivity for detecting small or
borderline nodes and extranodal soft-tissue disease.16,18 Using PET as a first-line investigation in place of conventional imaging techniques may improve the accuracy of staging as well as being
more cost effective. In one study of 18 patients with NHL and HD, PET
scanning increased the disease stage in three patients by detecting
lesions not previously identified by a variety of clinical and imaging
techniques.17
The role of PET for assessing marrow disease has not been addressed and
may further add to its value in staging lymphoma. We postulated that
increased uptake of FDG in marrow might correlate with the presence of
disease in patients at initial diagnosis. The purpose of this study was
to determine whether the intensity and distribution of FDG uptake in
the marrow could be used to accurately identify marrow infiltration.
| |
MATERIALS AND METHODS |
Patients.
Fifty consecutive patients with HD or NHL who were staged before
treatment by both PET scan and BM biopsy were prospectively recruited
into the study. The routine lymphoma staging procedure at our
institution involves thoracic and abdominal CT scan, whole-body FDG-PET, and a unilateral iliac crest marrow aspirate and trephine biopsy. In all patients the PET scan was performed within 4 weeks of
the marrow biopsy.
Marrow histology.
Marrow aspirates were stained with May-Grünwald-Giemsa. Trephine
biopsy samples were decalcified and stained with hematoxylin and eosin
and Gordon and Sweet's reticulin method. All biopsy samples were
stained with CD20 for B cells and CD3 for T cells. Where appropriate,
specimens were stained with CD15, CD30,  and  light chains, and
IgG, IgA, IgM heavy chains. The marrow biopsy samples were examined for
lymphoma infiltration by two hematologists and a histopathologist,
blinded to the PET scan result. The NHLs were classified according to
the Kiel and Revised European-American Lymphoma (REAL)
classifications.19
PET scanning.
18-Fluoride was produced in a Siemens RDS 112 cyclotron (Siemens CTI,
Knoxville, TN) by proton bombardment of a high-pressure water target.
FDG was synthesized by the method of nucleophilic substitution of a
precursor by 18  F . PET scans were performed after a
6-hour fast using an ECAT 951R whole body scanner (Siemens CTI). The
patients were injected with 350 MBq of [18F]-FDG and
imaged 30 to 45 minutes later with half-body images obtained by
acquiring 10 consecutive 5-minute images from the skull base to the mid
thigh. The complete sets of 310 image planes were reconstructed by
filtered back projection and smoothed in the axial direction to obtain
a single 3D dataset with a spatial resolution of 12 mm. Images were
viewed as a series of transaxial, coronal, and sagittal volume images.
Analysis of FDG uptake by marrow.
For the purposes of this study, the intensity and distribution of FDG
activity within the marrow was visually scored by three nuclear
medicine physicians independently. The marrow was assumed to be
abnormal where the uptake was equal to or greater than uptake into the
liver, provided the liver uptake was greater than background. In one
patient where there was negligible uptake within the liver, marrow
uptake was compared to uptake within soft tissue rather than using the
liver as the reference organ. The pattern of increased uptake was also
noted, with patients who appeared to have focal disease only within the
marrow differentiated from those with diffusely abnormal marrow
changes. Representative examples of cases with marrow uptake of
differing intensity (Fig 1) and
distribution (Fig 2) are shown.
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| Fig 1.
Coronal images are shown from three patients with
different degrees of marrow uptake on PET. FDG uptake within the marrow is seen on these sections in the thoracic spine (broken arrows) and
within the liver (solid arrow). The intensity of uptake was graded as
less than liver (A), equal to liver (B), or greater than liver (C),
with the marrow deemed to be abnormal where uptake was equal to or
greater than liver.
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| Fig 2.
The distribution of uptake within the marrow was noted.
Focal abnormality is seen within the lumbar spine in patient A (arrow), while patient B has diffuse marrow abnormalities.
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The kappa () statistic20 was used to measure
interobserver variability to assess the reproducibility of the visual
method used to assess marrow disease on PET. Where there were
differences in reporting between observers, if two reporters concurred
this was taken as the final PET report.
| |
RESULTS |
Fifty patients with NHL (38) and HD (12) were recruited into the study.
Forty-nine patients had lymph node, splenic, or soft-tissue extranodal
lymphoma masses shown by CT or clinical examination. All but 2 of these
49 patients had their nodal and/or extranodal disease
demonstrated by the FDG-PET scan. The 2 patients whose primary lymph
node disease did not accumulate FDG are discussed below. The remaining
patient, who had no clinical lymphadenopathy and a normal abdominal CT
scan, had intense uptake of FDG within the peritoneum and bowel due to
a diffuse infiltration by Burkitt's lymphoma cells. This patient has
been previously reported.12
There were 29 PET scans in which the marrow was regarded as having
normal FDG uptake. There were 21 PET scans in which the marrow was
considered to be abnormal: 16 of these patients had diffusely abnormal
marrow uptake, 3 of whom had focal areas of higher intensity within a
diffusely abnormal marrow. Five patients (3 diffuse large B-cell NHL, 2 HD) had focal areas of abnormality only, with the remainder of the
marrow showing normal FDG uptake.
Assessment of inter-observer agreement in interpretation of PET.
There was complete agreement between the three observers in 76% (22 of
29) of scans showing normal marrow uptake and 71% (15 of 21) of scans
showing abnormal uptake, either in a focal or diffuse pattern. There
was thus good overall agreement between observers, = 0.64.
In those patients who had PET scans that were discordant with biopsy
histology, all three observers agreed on the classification of marrow
uptake as normal or abnormal in 73% (8 of 11). Therefore, there is no
evidence that discordant results were a consequence of PET scans that
were more difficult to assess.
Patients with a concordant PET and routine iliac crest marrow biopsy
result.
In 39 patients there was concordance between the PET scan and the
routine iliac crest marrow biopsy (Table
1). In 26 patients there was
no increased FDG uptake within the marrow and the biopsy histology was
normal. In 13 patients increased marrow FDG uptake was associated with
histological evidence of marrow infiltration by lymphoma in the routine
iliac crest biopsy (11 NHL, 2 HD). Two of these patients demonstrated
the sensitivity of the PET technique: 1 patient with follicular
centroblastic centrocytic lymphoma who had low-volume, nodular marrow
disease (Fig 3A) and another patient with
T-lymphoblastic lymphoma, who had only 15% blast cells on marrow
aspirate and a modest interstitial infiltrate on trephine section (Fig
3B). Both had the marrow disease identified by increased FDG uptake.
Only 1 of the 5 patients with focal FDG uptake in an otherwise normal
marrow had, by chance, an area of high FDG accumulation ("hot
spot") biopsied by the routine marrow trephine, which confirmed NHL.
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| Fig 3.
Trephine biopsy sections. (A) A patient with follicular
centroblastic centrocytic lymphoma stained with hematoxylin and eosin showing low-volume, nodular disease (original magnification ×100). (B) A patient with T-lymphoblastic lymphoma stained with anti-CD3; cells with dark cytoplasm are CD3+ (original
magnification ×400). These photomicrographs show the low level of
lymphoma infiltration which in both cases was detected by PET.
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Patients with a discordant PET and routine iliac crest marrow biopsy
results.
In 11 patients the PET scan and marrow biopsy findings differed (Table
2). In 8 patients the PET scan showed focal
or diffuse increased FDG uptake, but the routine iliac crest marrow
biopsy specimen contained no evidence of lymphoma.
All four patients who had focal marrow disease on the PET scan but
histologically normal iliac crest marrow had normal FDG uptake at the
site of the biopsy. In that respect these patients could be classed as
concordant. In one of these patients subsequent biopsy of a "hot
spot" localized within the left humeral head confirmed nodular
sclerosing HD in the marrow (Fig 4). The
other 3 patients did not have additional biopsies, but the 2 patients with high-grade NHL had other evidence of stage IV disease, with pulmonary lymphoma deposits shown by PET and CT.
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| Fig 4.
PET images of a patient with areas of focal increased
uptake in marrow, most notably in the left humerus (solid arrow, A) and
in the thoracic spine (B). The marrow was not diffusely abnormal and
much of the axial skeleton exhibited FDG uptake less than in liver
(broken arrow).
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In the 4 patients with diffusely positive marrow on PET but normal
biopsies there was no other evidence indicating marrow infiltration.
The 2 patients with HD had the reactive myeloid hyperplasia
characteristic of some HD patients; this in itself may have increased
FDG uptake. The patients with T-cell and Ki-1+ lymphoma had
clinical stage IV and stage II disease, respectively. None of these 4 patients had additional marrow biopsies to confirm the absence of
disease.
Three patients had histologically demonstrated marrow disease that was
not detected by the PET scan. Two of these patients, with low- and
intermediate-grade NHL, had no FDG uptake into the site of their
primary lymph node disease. Therefore, it was predictable that the PET
scan would be unable to detect similar cells in the BM. In only one
patient with histologically demonstrated marrow lymphoma was the marrow
negative on PET when there was FDG uptake into another disease site, in
this case the spleen. This patient had mantle cell lymphoma confined to
spleen, marrow, and peripheral blood and is discussed further below.
| |
DISCUSSION |
In 39 of the 50 patients studied the PET scan correctly predicted the
result of the unilateral staging marrow biopsy. In an additional 6 patients, in whom the PET scan and marrow histology differed, it was
possible to predict, through careful interpretation of the PET scan,
that either the scan or the biopsy would be an unreliable tool for
diagnosing marrow disease. These included the 2 patients who had
primary lymph node sites which did not accumlate FDG and the 4 patients
with only focal marrow FDG uptake at sites distant from the iliac crest
biopsy (Table 2). These latter 4 patients all had normal FDG uptake at
the routine iliac crest biopsy site and all might well have had
lymphoma confirmed by a PET guided biopsy. This assumption is supported
by the one patient who had an initial iliac crest biopsy that was
negative, followed by a positive biopsy from a focal "hot spot"
within the left humeral head.
In the remaining 5 patients, representing 10% of the total studied,
the cause of the discrepancy between PET and biopsy was less certain.
In the 4 patients with diffuse PET+, biopsy marrows the explanation
may be either reactive hematopoietic changes within the marrow or
genuine marrow disease that was missed by the single, unilateral
biopsy. There was histological evidence to support myeloid hyperplasia
as the cause of increased FDG uptake in the two HD patients. The
alternative explanation, sampling error of patchy disease, has been
recognized to occur in between one third and one half of high-grade NHL
and HD patients.5-8
A unilateral staging marrow biopsy is in line with standard practice in
the United Kingdom.4 As this study is the first to examine
the ability of PET to identify marrow lymphoma it was not felt
appropriate to perform additional biopsies unless it would have altered
the intended treatment. This was the case in only one study patient.
In only one subject was the marrow negative with PET in the presence of
histological marrow disease, when there was FDG uptake into another
extranodal disease site. This patient, who represents the only
"false negative" PET result, had a number of unusual features. He
presented as a leukemic variant of mantle cell
lymphoma21,22 with a high peripheral white blood cell count
and splenomegaly but no clinical or CT detectable lymphadenopathy to
assess FDG uptake at lymph node disease sites. The marrow had an
interstitial infiltrate with B cells accounting for approximately half
the cell population. The spleen, which appeared to be the primary disease site, was grossly enlarged (15 cm by CT scanning) and displayed
high FDG uptake. The presence of increased FDG uptake within the spleen
but not within the marrow might be explained by the high density of
malignant lymphocytes in the spleen compared to the much lower volume
and density within the marrow, in a tumor with an inherently low FDG
uptake.
Although PET is increasingly being recognized as a valuable technique
for the primary staging of patients with HD and NHL, the
assessment of marrow infiltration by lymphoma using PET has not
previously been investigated. Since the earliest studies of FDG uptake
by lymphoma,23 FDG-PET has been found to be an effective method of staging these diseases which compares favorably with other
conventional imaging techniques and is more sensitive at detecting
extranodal disease than CT.12,16-18 In addition, the uptake
of FDG appears to correlate with histological grade as defined by the
International Working Formulation14,24-27 and the proliferative rate of the malignant cells,15,26 thus
providing a potential index of prognosis. It has been previously noted
that some low-grade NHLs may have low or absent FDG
uptake,25,26 which may limit the use of PET in these
lymphoma types. This was the case in the present study in two patients
who had no FDG uptake into their primary disease sites. One of these
patients, who had bulky lymph node disease, had mantle cell (diffuse
centrocytic) lymphoma, a lymphoma type that has been shown to have
highly variable FDG uptake.26 The other had centroblastic
centrocytic lymphoma.
Other imaging techniques used to assess primary diseases of BM and
infiltration by lymphoma have included magnetic resonance imaging (MRI)
and BM scintigraphy. MRI is able to diagnose marrow infiltration as
well as image nodal disease in lymphoma and thus may have an advantage
over CT,28 although direct comparison of CT with MRI for
nodal staging of lymphoma has been very limited.29 MRI is
more sensitive than biopsy in detecting BM infiltration by
lymphoma28,30 and is probably the imaging technique of
choice in the regional assessment of marrow. However, it is not
feasible to routinely assess the entire marrow with MR as is possible
with PET.
BM scintigraphy has the ability to image the entire marrow, but the low
uptake of conventional radioisotopes such as 99mTc colloids in the
reticuloendothelial cells in the marrow relative to the liver and
spleen create areas that are difficult to interpret. MRI appears to be
superior to colloid imaging in the detection of marrow disease in
lymphoma,30 but the use of either of these imaging
modalities in combination with biopsy is better than biopsy alone.
Specific antibodies directed against granulocytes and myeloid precursors labeled with radioisotopes have recently been developed to
image BM in patients with primary BM disease, leukemias, and lymphoma
as well as patients with metastases from solid tumors.31,32 Antibody imaging has lower uptake in liver and spleen than colloid scintigraphy and may therefore be more sensitive. In one study in
patients with lymphoma, antibody imaging appeared to correlate with the
presence of marrow infiltration on biopsy, but as all the patients
included had known BM disease, the specificity of the technique is
unknown. As with MRI and PET, increased uptake is also likely to occur
with marrow hyperplasia. There may be a problem with antibody response
to repeated injections of murine antibody with serial imaging, although
the incidence of this appears low and would not be a consideration in
the initial staging of patients.
The shortcomings of these existing noninvasive techniques to image the
BM mean that staging biopsy continues to be used despite its drawbacks.
Our data would suggest that additional information regarding marrow
disease may be obtained from the PET scan at diagnosis of lymphoma. The
scoring system used, although subjective, appears to be reproducible
with good agreement between three independent observers interpreting
the scans. Because the study was performed in patients undergoing
whole-body nonattenuated scans for the purpose of staging lymphoma,
quantitative estimates of marrow uptake of FDG were not possible.
Absolute quantitation requires arterial blood sampling, which is not
feasible or desirable in routine clinical imaging. Semi-quantitative
estimates such as standardized uptake values (SUV), which are derived
from attenuation-corrected images, may improve the definition of
abnormal areas by reducing subjective assessment. Furthermore,
attenuation correction may reduce reconstruction artifacts, including
an apparent decrease in tracer accumulation in central structures such
as axial marrow when compared with a superficial organ such as the
liver, which is a potential source for error in the present study.
However, attenuation correction requires extra transmission data to be acquired which, for each 10-cm axial field of view, would take an
additional 10 to 20 minutes using current technology. Therefore, it can
only be applied over selected regions and would be subject to the same
sampling errors as marrow biopsy. The ability to acquire simultaneous
transmission and emission data is currently being evaluated33 and whole-body attenuation correction methods
are likely to be in clinical use shortly. This will enable SUVs to be
calculated for sites of abnormal marrow uptake during retrospective analysis of the whole-body scan and should further improve the specificity of PET for detecting marrow disease.
This study suggests that visual interpretation of marrow FDG uptake
during whole-body PET scanning can identify marrow infiltration by
lymphoma with an accuracy which may be at least as reliable as
unilateral iliac crest biopsy. Furthermore, these data are acquired as
a byproduct of a minimally invasive procedure when PET is used for
routine lymphoma staging. On the basis of the data reported here we
conclude that, in patients whose involved lymph nodes accumulate FDG,
normal marrow appearances indicate normal marrow histology. On the
other hand, confirmatory marrow biopsies are indicated in all patients
with abnormal FDG uptake, using the PET scan to direct the site of
biopsy where appropriate.
| |
FOOTNOTES |
Submitted June 26, 1997;
accepted December 11, 1997.
Address reprint requests to Robert Carr, FRCP FRCPath, Department of
Haematology, United Medical and Dental Schools of Guy's and St
Thomas's, St Thomas' Hospital Campus, Lambeth Palace Rd, London, SE1
7EH UK.
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" is accordance with 18 U.S.C. section 1734 solely to indicate this fact.
| |
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