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Value of Ultrasound-Guided Core Biopsy in
the Diagnosis of Malignant Lymphoma
Aitor Ferna
´ndez de Larrinoa, MD,
1
Jose del Cura, MD,
2
Rosa Zabala, MD,
2
Elena Fuertes, MD,
1
Francisco Bilbao, MD,
1
Jose I. Lopez, MD
1
1
Department of Anatomic Pathology, Hospital de Basurto, Avda. de Montevideo 18, Bilbao, 48013 Spain
2
Department of Radiology, Hospital de Basurto, Avda. de Montevideo 18, Bilbao, 48013 Spain
Received 23 June 2006; accepted 2 April 2007
ABSTRACT: Purpose. Ultrasound-guided core needle
biopsy for the diagnosis and management of malig-
nant lymphomas is controversial and has not been
accepted as an alternative to surgical biopsy. We
investigate the clinical usefulness of this procedure in
a large series of patients.
Methods. Over a 5-year period (2000–2004), ultra-
sound-guided core needle biopsies were performed
in 102 malignant lymphomas. Five diagnostic catego-
ries were considered: large B-cell lymphomas (LBCL),
small B-cell lymphomas (SBCL), Hodgkin’s disease
(HD), T cell lymphomas, and miscellaneous. Surgical
excisional biopsy of the node was performed in 47
cases (46.1%) for diagnostic confirmation.
Results. The overall diagnostic accuracy of ultra-
sound-guided core needle biopsy was 88.2% (90/102).
SBCL (39), LBCL (36), HD (15), T cell lymphomas (5),
and miscellaneous (7) [including T cell–rich B cell (2),
natural killer cell (1), Burkitt’s lymphoma (1), and non-
Hodgkin’s lymphoma of the B cell type, NOS (3)] were
correctly diagnosed. Three HDs, 1 natural killer cell
lymphoma, 1 follicular lymphoma, and 1 LBCL were
not correctly diagnosed. The core needle biopsy did
not yield tumor tissue in 6 cases.
Conclusions. Ultrasound-guided core needle biopsy
is effective in the diagnosis of malignant lymphomas
and can be used as the first diagnostic approach in
selected clinical situations. V
V
C2007 Wiley Periodicals,
Inc. J Clin Ultrasound 35:295–301, 2007; Published
online in Wiley InterScience (www.interscience.
wiley.com). DOI: 10.1002/jcu.20383
Keywords: ultrasound; core needle biopsy; lymph-
adenopathy; malignant lymphoma
Image-guided core needle biopsy has become an
important tool in the diagnosis of superficial
and deep masses and can frequently avoid the
need for open biopsy.
1–3
However, it has not
gained general acceptance in the diagnosis of ma-
lignant lymphoma in lymph nodes because the di-
agnosis and subtyping of these neoplasms may be
limited by the small size of the specimen.
4
The first trials to diagnose malignant lym-
phoma using core needle biopsy (CB) were re-
ported 2 decades ago.
5–7
At the same time, fine
needle aspiration cytology procedures were also
implemented with similar objectives
8–11
as the
cytologic diagnosis benefitted from flow cytometry
techniques.
12–14
Although the diagnostic accuracy
of these techniques is high, traditional lymph
node excisional biopsy is still considered by most
pathologists as the method of choice in diagnosing
malignant lymphomas. Several authors have
reported excellent results with image-guided CB
of malignant lymphoma.
5–7,15–26
We present the results of ultrasound-guided
CB in a prospective series of 102 malignant
lymphomas.
MATERIAL AND METHODS
At our institution, imaging-guided CBs are rou-
tinely performed as a diagnostic approach to deep
and superficial tumor masses. During a 5-year
period (2000–2004), a total of 294 lymph nodes
were biopsied under ultrasound guidance, 79 of
them being malignant lymphomas, 113 nonlym-
phoid malignancies, and 102 reactive/inflamma-
tory diseases. In the same period, the spleen was
biopsied in 13 cases, 7 of which were malignant
lymphomas. The series also includes 16 malignant
lymphomas affecting various extranodal sites,
including the liver (4 cases), kidney (2 cases), and
Correspondence to: J. Lopez
'2007 Wiley Periodicals, Inc.
VOL. 35, NO. 6, JULY/AUGUST 2007—DOI 10.1002/jcu
295
bowel (1 case). Most cases of malignant lympho-
mas were referred from the hematology clinic.
The study was prospective, and the work-up
included a detailed clinical history and complete
imaging studies (sonography, CT, and MRI when
needed) for all patients.
Procedures were performed using a freehand
technique in all cases. A 4–7-MHz linear trans-
ducer connected o an ATL 3000 or ATL 5000
scanner (Philips Ultrasound 3000, Bothell, WA)
was used to guide the puncture in lesions located
in the head and neck, axilla, thorax, breast,
groin, and extremities (Figure 1A). When the
lesion was located in the abdomen or pelvis, a 2–5-
MHz convex array probe was used. After local
anesthesia with 1% lidocaine, the biopsies were
taken using an 18-gauge BioPince needle (Inter-V,
Gainesville, FL). The biopsy device offers the
possibility to select one of 3 different excursions
of the needle ranging from 1.3 to 3.3 cm. The lon-
gest possible throw that matched with the target
size was selected in every case (Figure 1B). When
the target was an adenopathy and a lymphoma
was clinically suspected, 4 to 5 specimens were
usually obtained trying to avoid the lymph node’s
hilium. When other organs were biopsied, the nee-
dle was preferably directed at the periphery of the
lesion, avoiding central areas, which are fre-
quently necrotic. The gun was always fired when
the point of the needle was placed outside but
close to the boundaries of the lesion in an attempt
to include the capsule in the specimen. Sonogra-
phy was used to verify the correct placement of
the needle through the target lesion.
The obtained tissue fragments were immedi-
ately immersed in cooled saline serum to delay
cellular autolysis, and then forwarded to the pa-
thology department for processing. The receiving
pathologist performed several imprints, and the
saline solution was centrifuged. Imprints were
stained with hematoxylin-eosin and the centrifu-
gate stained with Papanicolaou stain. Some
unstained slides were stored in alcohol for immu-
nohistochemical studies, when needed. Tissue
FIGURE 1. A 70-year-old female with a follicular lymphoma. (A) Sonogram shows a supraclavicular node. (B) Sonogram obtained during the
ultrasound-guided core biopsy shows the brightly echogenic needle through the node. (C) Cytologic imprint shows a monotonous small-sized
lymphoid cell population. (D) Histologic detail of small lymphoid cells showing scarce cytoplasm and hyperchromatic nuclei arranged in a diffuse
pattern of growth.
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JOURNAL OF CLINICAL ULTRASOUND—DOI 10.1002/jcu
cores were processed using routine techniques.
In selected cases, formalin-fixed, paraffin-embed-
ded material was retrieved for molecular analysis
[IgH, TcR, and t(14;18) MBR and JH regions].
Lymph node surgical excision was performed
in 47 cases (46.1%). In the 55 cases in which sur-
gery was not possible or not needed, the definitive
diagnosis was based on hematologic studies, clin-
ical course, previous history, and CB findings.
RESULTS
There was a male predominance in the series (65
males, 37 females) with a mean 6SD age of 70 6
20 years (range, 17–100 years). Location of
lesions and diagnostic categories are summarized
in Table 1. Malignant lymphomas involved lymph
nodes in 79 cases and presented as visceral
masses in 23 cases, 7 of which were in the spleen.
Head and neck (31 cases) and the axilla and groin
(16 and 14 cases, respectively) were most com-
monly affected, with the extremities being very
rarely involved with lymphoma.
No major complications were observed after
CB. Minor hematomas and local pain were occa-
sionally reported, but they resolved spontane-
ously. Post-CB necrosis was found in a splenic
mass but was not directly related to the proce-
dure. Malignant seeding along the needle tract
was not detected.
The diagnostic work-up involved cytologic, his-
tologic, and immunohistochemical studies in all
cases. Molecular studies were performed in 11
cases. Imprints and cytocentrifugates showed
crushing artifacts in lymphoid cells. However,
they were helpful in cases of suboptimal histopa-
thologic slides. Overall, the diagnostic accuracy of
CB in the diagnosis of malignant lymphoma was
88.2% (90/102). There were no false positive cases
in the series. Discordant diagnoses are listed in
Table 2. Three cases of Hodgkin’s disease, 1 natu-
ral killer (NK) cell lymphoma, 1 follicular lym-
phoma, and 1 large B cell lymphoma were not cor-
rectly diagnosed. Additionally, the diagnosis could
not be made in 6 cases due to the fact that the
involved lymph node areas were not adequately
sampled by the radiologist. Interestingly, all the
discordant cases were located superficially in the
neck, axilla, or groin, and most of them (9 out of
12) occurred in the first 2 years of the study.
Small B Cell Lymphoma (39 Cases)
For this type of lymphoma, correlation with sur-
gical/excisional specimens was available in 13
cases (33.3%). Lymph nodes from the head and
neck, including supraclavicular area, were the
most frequently affected (11 cases). Other loca-
tions included the groin (6 cases), axilla (5 cases),
retroperitoneum (4 cases), abdomen (3 cases),
and pelvis, kidney, and breast (1 case each). Sali-
vary glands (parotid and submaxillary) were spe-
cifically affected by this category of lymphomas (6
cases).
Follicular lymphomas amounted to 28 cases
(71.8%), grade 1 cases being the most common
subgroup. Typical cytology and histology and B
cell lineage immunohistochemical markers were
invariably present. In addition, the double bcl-2/
bcl-6–positive immunostaining specifically de-
fined this subcategory. t(14;18) was positive in
6 cases and negative in 5 cases in the molecular
analysis. A total of 7 cases were diagnosed as
small B cell lymphoma, NOS, one of them show-
ing positive IgH rearrangement. Chronic lympho-
cytic lymphoma/leukemia was diagnosed in 3
cases (CD5 and CD23 positivity), and MALT lym-
phoma was diagnosed in 1 case.
Artifacts were not particularly important in
this category, and imprints and cytocentrifugates
displayed with precision the nuclear characteris-
tics in most cases.The histopathologic diagnosis
in this group could not be obtained in 4 cases.
The radiologist obtained nondiagnostic material
in 3 cases. Only one case of follicular lymphoma
was erroneously diagnosed as follicular hyperpla-
sia by the pathologist due to the scarcity of the
TABLE 1
Clinicopathologic Data in 102 Cases of Malignant
Lymphoma Diagnosed on Ultrasound-Guided Core
Needle Biopsy
n(%)
Organ involved
Lymph nodes 79 (77.5)
Spleen 7 (6.8)
Extranodal 16 (15.7)
Location
Head and neck (including supraclavicular fossa) 31 (30.4)
Axilla 16 (15.6)
Groin 14 (13.7)
Viscera 14 (13.7)
Spleen 7
Liver 4
Kidney 2
Bowel 1
Abdomen (extravisceral) 11 (10.8)
Thorax (including breast) 6 (5.9)
Pelvis 2 (1.9)
Extremities 1 (0.9)
Diagnostic categories
Small B cell lymphoma 39 (38.2)
Large B cell lymphoma 36 (35.3)
Hodgkin’s disease 15 (14.7)
T cell lymphoma 5 (4.9)
Others 7 (6.9)
CORE BIOPSY OF MALIGNANT LYMPHOMAS
VOL. 35, NO. 6, JULY/AUGUST 2007—DOI 10.1002/jcu
297
material obtained, which made a complete immu-
nohistochemical study impossible. The diagnostic
accuracy in this group was 89.7%.
Large B Cell Lymphoma (36 Cases)
For this group of lymphomas, correlation with
surgical/excisional specimens was available in 16
cases (44.4%). Lymph nodes in the abdomen (7
cases) and head and neck (6 cases) were the most
commonly affected. Other locations included the
axilla (5 cases), groin (3 cases), thorax (2 cases),
retroperitoneum (2 cases), and breast and arm (1
case each). Interestingly, more than half of lym-
phomas with viscera in our series (9 out of 14,
64.3%) belonged to this category. Among them,
spleen (6 cases), liver (2 cases), and kidney (1
case) involvement were seen.
CBs showed a diffuse lymphoid infiltrate com-
posed of large cells with round nuclei and one or
more nucleoli, as expected in this subtype of lym-
phomas. When the lymphoma involved a viscera,
its normal histology could be recognized in some
areas, sometimes intermingled with the neoplas-
tic lymphoid infiltrate. B cell lineage markers
were positive in all cases. Artifacts were seen at
the periphery of cores, and cell morphology and
immunostaining in these areas had to be eval-
uated with caution.
The diagnostic accuracy of CB in this group
was 94.6%. In fact, the correct diagnosis could
not be reached in only 2 cases. The radiologist
obtained inadequate material in 1 case, and the
pathologist found extensive necrosis in another.
Hodgkin’s Disease (15 Cases)
Correlation with excisional biopsy specimens was
available in 7 cases (47%). Nodular sclerosis (6
cases), mixed cellularity (4 cases), and nodular
lymphocytic predominance (1 case) subtypes were
found. The specific subtype could not be identified
in 4 cases due to the fact that the excisional biopsy
was not performed in these cases.
The diagnostic accuracy in this group was
73.4% (Table 2). The diagnosis of Hodgkin’s dis-
ease greatly depends on the identification of typi-
cal Reed-Sternberg cells, which is a problem
when evaluating small tissue fragments such as
cores.
T Cell Lymphoma (5 Cases)
Correlation with excisional biopsy material ws
available in 4 cases (80%). Aside from the liver (2
cases), lymph nodes in the axilla, groin, and
thorax (1 case each) were involved. There were 4
cases of peripheral T cell lymphoma and 1 case of
chronic lymphocytic leukemia of the T cell type.
Nuclear irregularities and CD3 positive immuno-
staining were typically present. In our experi-
ence, cytologic material was especially useful in
identifying the peculiar nuclear shape of tumor
cells in this category. There was no discrepancy
between CB and excisional biopsy.
Miscellaneous (7 Cases)
Table 3 summarizes the results in this group.
Correlation with excisional biopsy was possible
in 3 cases (42.8%). CB diagnosis was incorrect in
1 NK cell lymphoma and in 1 T cell–rich B cell
lymphoma.
DISCUSSION
In recent years, percutaneous image-guided CB
has been used increasingly in the diagnosis of
lymph node pathology as an alternative to surgi-
TABLE 2
Diagnostic Discrepancies in CB Diagnosis of Malignant Lymphoma (12 Cases)
Case Age/Sex Location CB Diagnosis Final Diagnosis Discordance
1 48/M Groin Nonspecific changes Follicular NHL, grade 1 Inadequate material
2 17/M Neck Nonspecific changes HD, nodular sclerosis Inadequate material
3 72/F Axilla Nonspecific changes LBCL Inadequate material
4 65/M Axilla Necrotic tissue LBCL Insufficient sampling
5 56/F Groin Benign tissue, NOS T-cell rich B-cell NHL Inadequate material
6 79/F Neck Benign tissue, NOS Follicular NHL, grade 1 Inadequate material
7 81/M Axilla Lymphoid proliferation NK cell lymphoma Insufficient sampling
8 40/M Groin Reactive/lymphoma HD, mixed cellularity Insufficient sampling
9 59/M Groin Benign tissue, NOS Follicular NHL, grade 2 Inadequate material
10 48/M Axilla Lymphoid proliferation HD-LPN Insufficient sampling
11 50/M Neck B cell lymphoma HD, nodular sclerosis Insufficient sampling
12 47/M Groin Lymphoid hyperplasia Follicular NHL, grade 1 Insufficient sampling
Abbreviations: HD, Hodgkin’s disease; HD-LPN, Hodgkin’s disease, lymphocytic predominance, nodular type; LBCL, large B cell lymphoma;
NHL, non-Hodgkin’s lymphoma, NK, natural killer.
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cal biopsy, particularly if the nodes are deep-
seated or if the clinical condition of the patient is
severely impaired. Sonography and CT show sim-
ilar success when in the hands of an experienced
operator, but sonography is usually preferred
because of its real-time capability.
The widespread use of this technique has
detractors among pathologists, because the scar-
city of the obtained material may make the diag-
nosis and/or subtyping of malignant lymphomas
more difficult.
4
Table 4 summarizes the accumu-
lated experience in this domain and reflects that
the diagnostic concordance between CB and sur-
gical biopsy samples is high (71%–89%). These
data support a more generalized use of this proce-
dure. In fact, de Kerviler et al
17
concluded in
their study on 194 patients that the diagnostic
approach of lymphoma should now be based on
minimally invasive techniques, and Sklair-Levy
et al,
24
after studying 114 cases of lymphoma
using this method, state that image-guided core-
needle biopsy should be considered as a first-step
method in the diagnosis of patients with superfi-
cial lymphadenopathies. Other authors
23
favor
its use in deep masses that would require gene-
ral anesthesia for surgical removal, and still
others
7,25
advise it in the absence of palpable su-
perficial lymph nodes.
Sonographic detection of superficial lymph
nodes was first reported 2 decades ago;
27
since
then, ultrasound-guided needle biopsy has shown
good results in various sites, including the medi-
astinum,
28,29
head and neck,
30
soft tissues,
3
and
spleen.
31
CT has also been used to guide needle
biopsies of the liver,
32
spleen,
33
and pelvis and
retroperitoneum.
34
Image-guided needle biopsy
has also been successfully applied in pediatric
patients.
35
In our experience, CB worked best in the
LBCL group. Indeed, the identification of a dense
population of large lymphoid cells with B cell
immunophenotype in tissue cores is usually suffi-
cient to confirm the diagnosis. We found some-
what similar results in the SBCL group, although
small neoplastic lymphocytes may be mistaken
for nonneoplastic elements if the tissue sample
contains both populations. The presence of B cell
lineage markers, together with the combined pos-
itivity for bcl-2 and bcl-6 in lymphoid cells, is
diagnostic of follicular lymphoma. However, this
combined immunostaining is not always unequiv-
ocal, particularly with bcl-2 and bcl-6 antibodies,
which explains some incomplete diagnoses in our
series. Small cells with CD5 and CD23 positivity,
in addition to the clinical setting, are diagnostic
of lymphocytic lymphoma/leukemia. As reported
previously,
23–25
HD is the most problematic diag-
nosis in CB in our series. The varied histologic
approaches of this disease, the scarcity of the
material for diagnosis, and the frequent absence
of Reed-Sternberg cells in the submitted material
are responsible for these difficulties. Though lim-
ited, our experience in the CB diagnosis of T cell
lymphomas is satisfactory. Nuclear peculiarities
of T cells and CD3-positive immunostaining are
crucial in its recognition. We have not found any
other reports on the diagnosis of T cell lymphoma
in CB, but Yao et al,
9
in their series of 33 cases,
reported that fine needle aspiration cytology is
TABLE 4
Series of Image-Guided CB in Malignant Lymphoma
Study Year
No. of
Cases
Imaging
Guidance
Overall
Diagnostic
Accuracy
of CB
Kalkner et al
5
1994 129 Ultrasound 87%
Ben-Yehuda et al
6
1996 100 CT 78%
Pappa et al
7
1996 106 CT/Ultrasound 83%
Zinzani et al
15
1998 55 Ultrasound 87%
Zinzani et al
16
1999 83 CT/Ultrasound 81%
de Kerviler et al
17
2000 158 CT/Ultrasound 88%
Sklair-Levy et al
18
2000 49 CT 71.5%
Demharter et al
19
2001 65 CT 89.2%
Screaton et al
20
2002 66 Ultrasound 80%
Agid et al
21
2003 267 CT 82.5%
Goldschmidt et al
22
2003 130 CT 75.4%
Balestreri et al
23
2005 137 CT 87%
Sklair-Levy et al
24
2005 114 CT/Ultrasound 84.2%
Li et al
25
2005 80 CT 76.2%
Ravinsky et al
26
2005 28 CT 82%
Present study — 102 Ultrasound 88.2%
TABLE 3
Miscellaneous Group of 7 Miscellaneous Malignant Lymphomas Diagnosed on CB
Case Age/Sex Location CB Diagnosis Excisional Diagnosis
1 23/F Ileon Burkitt’s lymphoma ND
2 55/M Spleen NHL, B cell type ND
3 78/M Mesentery NHL, B cell type ND
4 54/M Neck NHL, high-grade NHL, B cell type (autopsy)
5 56/F Groin Benign tissue, NOS T–cell rich B cell lymphoma
6 48/M Retroperitoneum T cell– rich B cell lymphoma ND
7 81/M Axilla Lymphoid proliferation NK cell lymphoma
Abbreviations: ND, not done; NHL, non-Hodgkin’s lymphoma; NK, natural killer.
CORE BIOPSY OF MALIGNANT LYMPHOMAS
VOL. 35, NO. 6, JULY/AUGUST 2007—DOI 10.1002/jcu
299
an accurate diagnostic method. The low fre-
quency of T cell– rich B cell and NK cell lympho-
mas makes diagnosis very difficult and depend-
ent on the quality of the submitted material.
Finally, Burkitt’s lymphoma diagnosis is favored
by the typical clinical setting and histology.
Molecular analysis in our series was per-
formed only to help the pathologic diagnosis
and was particularly helpful in distinguishing
follicular lymphoma from nonneoplastic lymphoid
proliferations.
Ultrasound-guided needle biopsy is a useful
method in the diagnosis of malignant lymphoma,
but optimal results require experienced radiolog-
ists and pathologists. In fact, 9 out of 12 diagnos-
tic failures occurred in the first 2 years of the
study. Tight collaboration between clinicians,
radiologists, and pathologists is the key to suc-
cess. CB is especially useful in patients who are
in poor clinical condition or in any situation that
prevents an open surgical biopsy. Nonetheless,
we believe that open lymph node biopsy still
remains the standard procedure for the complete
histopathologic diagnosis of some malignant
lymphomas.
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