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Cervical Lymphadenopathy: Sonographic
Differentiation between Tuberculous Nodes
and Nodal Metastases from Non–Head and
Neck Carcinomas
Michael Ying, MPhil,1 Anil T. Ahuja, FRCR,1 Rhodri Evans, FRCR,1,* Walter King, MD,2
Constantine Metreweli, FRCR1
1
Department of Diagnostic Radiology and Organ Imaging, Prince of Wales Hospital, Shatin,
New Territories, Hong Kong
2
Department of Surgery, Prince of Wales Hospital, Shatin, New Territories, Hong Kong
Received 15 September 1997; accepted 12 February 1998
ABSTRACT: Purpose. Clinical examination alone cannot differentiate between cervical tuberculous lymphadenitis and cervical nodal metastases from non–
head and neck (NHN) carcinomas because the
distributions of involved lymph nodes are similar. We
evaluated the sonographic features of cervical lymph
nodes that could be used to differentiate between the
2 categories of nodes.
Methods. We retrospectively reviewed sonograms
of abnormal cervical lymph nodes in 47 patients with
proven cervical tuberculous lymphadenitis and in 22
patients with proven nodal metastases from NHN carcinomas.
Results. Abnormal nodes in tuberculous lymphadenitis and nodal metastases from NHN carcinomas
were commonly found in the supraclavicular fossa
(15% and 38%, respectively) and the posterior triangle
(70% and 41%, respectively). Statistically significant (p
< 0.05) features for differential diagnosis were lymph
nodes’ longest diameter, echogenicity, short-to-long
axis ratio, appearance of surrounding soft tissues, and
presence of intranodal cystic necrosis, matting, and
posterior enhancement. Nodal size, echogenicity,
presence of an echogenic hilum, calcification, coagulation necrosis, and sharpness of borders helped in
identifying the abnormal lymph nodes.
Conclusions. Sonographic features that helped to
differentiate between the 2 categories of nodes were
shape, edema of surrounding soft tissue, homogene*Current address: Radiology Department, Morriston Hospital,
Morriston, Swansea SA6 6NL, United Kingdom
Correspondence to: A. T. Ahuja
© 1998 John Wiley & Sons, Inc.
VOL. 26, NO. 8, OCTOBER 1998
CCC 0091-2751/98/080383-07
ity, intranodal cystic necrosis, matting, and posterior
enhancement. © 1998 John Wiley & Sons, Inc. J Clin
Ultrasound 26:383–389, 1998.
Keywords: ultrasonography; cervical lymph nodes; tuberculosis; infraclavicular carcinomas
T
he distribution of enlarged lymph nodes is an
important clue in deciding the possible causes
of cervical lymphadenopathy, but when the distribution is similar in different diseases, clinical
examination alone cannot distinguish between
the various causes.1 Sonography of cervical lymph
nodes is more accurate than clinical examination
owing to its high sensitivity, but it is limited by its
low specificity; therefore, to increase specificity,
sonography is usually combined with fine-needle
aspiration biopsy.2 The sonologist, however, must
be aware of the sonographic features that may
help to identify the cause of cervical lymphadenopathy because fine-needle aspiration biopsy is
sometimes nondiagnostic and may not be available in all centers. Thus, evaluation of the sonographic appearances of abnormal cervical lymph
nodes may be helpful in the differential diagnosis.
Tuberculous lymphadenitis is common in
southeast Asia. With the increasing incidence of
acquired immunodeficiency syndrome and associated tuberculosis, it is necessary to make a
prompt, early diagnosis. Tuberculous lymphadenitis is usually found in the supraclavicular
fossa and posterior triangle of the neck,3–7 but
383
YING ET AL
non–head and neck (NHN) carcinomas, such as
carcinomas of the breast, lung, gastrointestinal
tract, and cervix, also commonly metastasize to
supraclavicular lymph nodes.8,9 Because NHN
carcinomas and tuberculous lymphadenitis tend
to involve lymph nodes in similar regions, the distribution pattern of diseased lymph nodes cannot
help to narrow the differential diagnosis. The sonography literature does not discuss the specific
features of cervical lymph nodes that help to differentiate between these 2 conditions. Therefore,
the present study evaluated the sonographic features of cervical lymph nodes that could be used
to differentiate between nodal metastasis from
NHN carcinoma and tuberculous lymphadenitis.
PATIENTS AND METHODS
We retrospectively reviewed sonograms of the
neck of 47 patients (17 males and 30 females;
mean age, 34 years) with proven tuberculous
lymphadenitis and of 22 patients (10 males and
12 females; mean age, 50 years) with proven
nodal metastases from NHN carcinomas. All patients were Asian. All scans were performed with
an SSD-650 ultrasound scanner (Aloka, Tokyo,
Japan) with a 7.5-MHz linear-array transducer
and a 10-MHz sector transducer with a built-in
water bath. Among the 22 patients with NHN
carcinomas, the primary carcinoma was in the
breast in 10 patients, the lung in 11 patients, and
the cervix in 1 patient. None of these patients had
previously had radiotherapy to the neck. All patients in both groups had undergone ultrasoundguided fine-needle aspiration biopsy of the largest
node, and if the result was inconclusive, an excisional biopsy of the same node had been performed. Cytologic and/or histologic investigations
proved all aspirated or biopsied lymph nodes to be
metastases from NHN carcinoma or tuberculous
lymphadenitis. In each patient, all other lymph
nodes with sonographic features similar to those
of the aspirated or biopsied node were considered
to be involved by the same pathologic process.
The cervical lymph nodes were classified into 8
regions using a method similar to that of Hajek et
al11: submental; submandibular; parotid; upper
cervical, ie, above the hyoid bone and along the
common carotid artery and the internal jugular
vein; middle cervical, ie, between the hyoid bone
and the cricoid cartilage and along the common
carotid artery and internal jugular vein; lower
cervical, ie, below the cricoid cartilage and along
the common carotid artery and internal jugular
vein; supraclavicular fossa; and posterior triangle, also known as the accessory chain.
384
Lymph nodes were assessed using established
sonographic criteria7,10: distribution, size, shape,
presence of an echogenic hilum, internal architecture, homogeneity, echogenicity, sharpness of
borders, posterior enhancement, and ancillary
features such as matting and status of surrounding soft tissues.
Lymph node shape was assessed by the shortto-long axis ratio (S/L). An S/L of less than 0.5
indicated an elongated or elliptical node, whereas
an S/L of 0.5 or more indicated an oval or round
node.12
The internal architecture of lymph nodes was
assessed for the presence of calcifications, coagulation necrosis, and cystic necrosis. Coagulation
necrosis is an ischemic degeneration found in
lymph nodes with malignancy or inflammation.13
Coagulation necrosis is less echogenic than an
echogenic hilum and is not continuous with the
surrounding fat.13,14 Areas of coagulation necrosis tend to be round or oval (ie, S/L 艌 0.5),
whereas a hilum is usually linear or elliptical (ie,
S/L < 0.5).13 Lymph nodes were considered to be
homogeneous when they had no calcifications, coagulation necrosis, or cystic necrosis.
The echogenicity of lymph nodes was determined by comparison with the adjacent muscle(s)
and was classified as hypoechoic, isoechoic, or hyperechoic. Lymph nodes were considered to have
posterior enhancement when the structures posterior to the node were more echogenic than
neighboring structures.
Matting was considered to be clumping of multiple abnormal lymph nodes with no normal soft
tissue between them.
Edema of surrounding cervical soft tissues appeared hypoechoic and was associated with a loss
of fascial planes. All nodes with edema of adjacent
soft tissue were considered abnormal.
The mean sizes of nodal metastases from NHN
carcinomas and tuberculous lymphadenitis were
compared using Student’s t-test. The sonographic
features of tuberculous lymphadenitis and nodal
metastases from NHN carcinomas were compared using the chi-squared test. A p value of less
than 0.05 was considered statistically significant.
RESULTS
A total of 315 lymph nodes were involved by tuberculosis, and 114 lymph nodes were involved by
metastatic NHN carcinoma. Involved nodes were
most commonly found in the supraclavicular fossa
(15% of tuberculous nodes and 38% of NHN metastases) and the posterior triangle (70% of tuberJOURNAL OF CLINICAL ULTRASOUND
CERVICAL LYMPHADENOPATHY
culous nodes and 41% of NHN metastases) (Figure 1).
The size of lymph nodes (long axis × short axis)
involved by tuberculosis ranged from 9 × 3 mm to
42 × 20 mm, and nodal metastases ranged from 7
× 5 mm to 42 × 33 mm. The mean short axis of the
lymph nodes involved by tuberculosis (10.2 mm)
was not significantly different than that of nodal
metastases (10.0 mm) (p > 0.05). However, the
difference in the mean long axis of lymph nodes
involved by tuberculosis (19.0 mm) and that for
nodal metastases (15.6 mm) was statistically significant (p < 0.05).
Table 1 shows the numbers, sizes, and sonographic features of lymph nodes involved by
metastatic NHN carcinoma and those involved by
tuberculosis and gives the significance of differences between the 2 diseases.
The significant sonographic features for differential diagnosis included echogenicity, sharpness
of border, shape, edema of surrounding soft tissue, homogeneity, intranodal cystic necrosis, matting, and posterior enhancement. The majority of
lymph nodes involved by either tuberculosis or
metastatic NHN carcinoma were hypoechoic
(100% and 92%, respectively) and had sharp borders (62% and 74%, respectively). Therefore, although the difference in echogenicity was statistically significant, it was not large enough to be
clinically useful. Only 5% of nodal metastases had
an S/L of less than 0.5, whereas 21% of tuberculous nodes had an S/L of less than 0.5 (Figure 2).
Tuberculous lymphadenitis had a higher incidence of abnormal surrounding soft tissues (49%),
cystic necrosis (60%) (Figures 2 and 3), and mat-
ting (59%) (Figure 4) than did nodal metastases
(4%, 8%, and 8%, respectively). Heterogeneous
lymph nodes were commonly found in tuberculous
lymphadenitis (64%), whereas nodal metastases
were predominantly homogeneous (88%). Posterior enhancement was more common in tuberculous lymphadenitis (22%) than in nodal metastases (4%) (Figure 3).
The sonographic features that were insignificant to the differential diagnosis included the
presence of an echogenic hilum, intranodal calcifications, and intranodal coagulation necrosis.
Lymph nodes involved by either tuberculosis or
metastatic NHN carcinoma commonly had no hilum (86% and 87%, respectively). Calcifications
and coagulation necrosis were rarely found in
lymph nodes involved by tuberculosis (1% and
6%, respectively) or in nodal metastases (0% and
7%, respectively).
DISCUSSION
Cervical tuberculous lymphadenitis and cervical
nodal metastases from NHN carcinomas cannot
be differentiated solely on the basis of the distribution of involved lymph nodes. In this study, the
majority of lymph nodes involved by tuberculosis
were found in the supraclavicular fossa and the
posterior triangle, consistent with previous reports.3–7 However, these were also the most common sites of NHN metastases, in contrast to previous reports in which only supraclavicular
lymph nodes were involved by metastases.8,9 This
difference is probably due to the fact that in this
FIGURE 1. Schematic of the neck showing the distribution of tuberculous lymph nodes (white bars) and nodal metastases from non–head and neck
carcinomas (black bars).
VOL. 26, NO. 8, OCTOBER 1998
385
YING ET AL
TABLE 1
Sonographic Features of 315 Tuberculous Lymph Nodes and 114 Nodal Metastases from
Non–Head and Neck Carcinomas
Number of Lymph Nodes (%)
Sonographic Feature
Size
Range, mm
(long axis × short axis)
Mean short axis, mm
Mean long axis, mm
Echogenicity*
Hypoechoic
Isoechoic
Hilum
Present
Absent
Calcification
Present
Absent
Coagulation necrosis
Present
Absent
Nodal border
Sharp
Not sharp
Shape
S/L < 0.5
S/L 艌 0.5
Surrounding tissues
Normal
Abnormal
Homogeneity
Homogeneous
Heterogeneous
Cystic necrosis
Present
Absent
Matting
Present
Absent
Posterior enhancement
Present
Absent
Tuberculous
Lymphadenitis
Nodal
Metastasis
9 × 3 to 42 × 20
10.2
19.0
7 × 5 to 42 × 33
10.0
15.6
Significance of Difference
between the 2 Diseases
NS
p < 0.05
315
0
(100%)
(0%)
105
9
(92%)
(8%)
p < 0.0001
45
270
(14%)
(86%)
15
99
(13%)
(87%)
NS
4
311
(1%)
(99%)
0
114
(0%)
(100%)
NS
18
297
(6%)
(94%)
8
106
(7%)
(93%)
NS
195
120
(62%)
(38%)
84
30
(74%)
(26%)
p < 0.03
67
248
(21%)
(79%)
6
108
(5%)
(95%)
p < 0.0001
160
155
(51%)
(49%)
110
4
(96%)
(4%)
p < 0.0001
112
203
(36%)
(64%)
100
14
(88%)
(12%)
p < 0.0001
188
127
(60%)
(40%)
9
105
(8%)
(92%)
p < 0.0001
185
130
(59%)
(41%)
9
105
(8%)
(92%)
p < 0.0001
68
247
(22%)
(78%)
5
109
(4%)
(96%)
p < 0.0001
Abbreviations: NS, not significant (p 艌 0.05); S/L, short-to-long axis ratio.
*
No nodes in either group were hyperechoic.
study, patients with NHN carcinoma were included regardless of whether they had abnormal
supraclavicular lymph nodes, whereas previous
studies included only patients who had abnormal
supraclavicular lymph nodes, which resulted in
selection bias.
The sonographic features of cervical tuberculous lymphadenitis and cervical nodal metastases
from NHN carcinomas can be grouped into three
general categories: (1) features that indicated abnormality but were not specific, (2) features that
favored metastasis from NHN carcinoma, and (3)
features that favored tuberculous lymphadenitis.
The sonographic features of nodal size, echogenicity, presence of an echogenic hilum, calcification, coagulation necrosis, and sharpness of
borders were generally not helpful in the differ386
ential diagnosis. Although previous studies
showed nodal size to be of little value in differentiating benign from malignant nodes,15,16 we
found a statistically significant difference in the
mean long axes of lymph nodes involved by tuberculosis and those involved by metastasis (p <
0.05). Unfortunately, this difference was not large
enough to be clinically useful.17 Echogenicity was
unhelpful because the majority of lymph nodes
involved by either disease were hypoechoic. Likewise, the presence of an echogenic hilum was not
helpful because the majority of lymph nodes had
no hilum. Calcification in nodal metastasis is generally rare, except in nodal metastases from papillary carcinoma of the thyroid.18,19 Calcification
may be found in tuberculous lymphadenitis, but it
is not pathognomonic for tuberculosis.5 In this
JOURNAL OF CLINICAL ULTRASOUND
CERVICAL LYMPHADENOPATHY
FIGURE 2. Longitudinal sonogram of an oval lymph node in the posterior triangle of the neck with extensive
intranodal cystic necrosis (black arrows). This appearance is suggestive of tuberculous lymphadenitis.
study, calcification was not a useful distinguishing feature because the majority of lymph nodes
had no calcification. Similarly, coagulation necrosis occurred too infrequently to be useful. Finally,
previous reports have described nodal metastases
as having sharp, well-defined borders and inflammatory lymph nodes as having poorly defined borders.19,20 In this study, the majority of tuberculous lymph nodes and nodal metastases had
sharp borders. Although sharpness of borders
was found to be a statistically significant feature,
it is unlikely to be clinically useful.
Sonographic features that favored metastasis
from NHN carcinoma were normal surrounding
soft tissues, absence of intranodal cystic necrosis,
absence of matting, and homogeneity. Compared
with tuberculous lymphadenitis, almost twice as
many nodal metastases had normal surrounding
soft tissues, and more than twice as many showed
no intranodal cystic necrosis and/or were homo-
FIGURE 3. Longitudinal sonogram of the posterior triangle of the neck showing tuberculous lymph nodes with
intranodal cystic necrosis (white arrows). Note the enhancement distal to the lymph nodes (black arrows).
VOL. 26, NO. 8, OCTOBER 1998
387
YING ET AL
FIGURE 4. Longitudinal sonogram of the posterior triangle of the neck showing multiple hypoechoic tuberculous lymph nodes matted together without normal intervening soft tissue.
geneous. Matting of lymph nodes, which was seen
in 59% of tuberculous lymph nodes, occurred in
only 8% of nodal metastases.
Sonographic features that favored tuberculous
lymphadenitis were more striking. These were an
S/L of less than 0.5, abnormal surrounding soft
tissues, heterogeneity, intranodal cystic necrosis,
matting, and posterior enhancement. In agreement with van Overhagen et al,21 who reported
that the S/L of malignant nodes was greater than
that of benign nodes, we found that an S/L of less
than 0.5 occurred more often in tuberculous
lymphadenitis than in nodal metastases. We also
found that 49% of tuberculous lymph nodes
showed abnormal surrounding soft tissues, which
included edema or induration of the subcutaneous
tissue and/or adjacent muscle; only 4% of nodal
metastases showed this feature. The high incidence of heterogeneity seen in tuberculous
lymphadenitis (64%) probably resulted from the
high incidence of intranodal cystic necrosis (60%).
Intranodal cystic necrosis is common in tuberculous lymphadenitis and can also be identified by
CT, on which it appears as a central low-density
area with rim enhancement.22 While intranodal
cystic necrosis may occur in malignant lymph
nodes,23 such an occurrence in our study was infrequent. Matting of lymph nodes is another common feature in tuberculous lymphadenitis,6,24
and in cases of tuberculous lymphadenitis in
which there has been considerable periadenitis,
the involved lymph nodes will be matted together
with fibrous tissue.3 Finally, except for lymph
nodes affected by non-Hodgkin’s lymphoma,17,25
388
posterior enhancement is not frequently seen in
nodal metastases because they are composed of
tumor cells separated by supportive tissue that
produces numerous interfaces. Only 4% of the
nodal metastases in this study showed posterior
enhancement. However, 22% of tuberculous
lymph nodes showed this feature, an incidence
that again may be due to the high incidence of
intranodal cystic necrosis.
Our study shows that of all the sonographic
criteria previously described for abnormal lymph
nodes, the only ones likely to help differentiate
between tuberculous lymphadenitis and nodal
metastasis from NHN carcinoma are an S/L of
less than 0.5 versus an S/L of 0.5 or more, abnormal versus normal surrounding soft tissue, heterogeneity versus homogeneity of the node, and
presence versus absence of intranodal cystic necrosis, matting, and posterior enhancement.
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