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5 Sonography ofLymph Nodes intheNeck
Fig. 5.17 Stage III non-
tuberculous CLN with
“parchment-like” appearance
of the overlying skin and a
livid discoloration
67
Fig. 5.18 In stage IV of
non-tuberculous disease, the
lesion stulizes to the skin
surface causing a sinus-like,
draining wound and
echogenic intrinsic reexes
with and without acoustic
shadows
vascularity depending on the rate of growth and the
development of necrotic areas, which cause perfusion
defects that may mimic the Doppler US appearance of
TCLNs. However, evaluation of the vascular pattern of
CLNs may not distinguish between different benign nodal
diseases, as their vascular patterns vary with the stage of
disease [3, 87].
Qualitative/quantitative elastographic assessment No
investigation has yet been done on this research eld.
68
Fig. 5.19 End-stage
non-tuberculous
mycobacterial infection with
multiple intranodal
calcications, which is rather
uncommon in juvenile CLNs
and can only be found in
metastatic nodes from
papillary carcinoma of the
thyroid in children
J. E. Meyer
5.1.4 Epstein-Barr Virus (EBV)-Triggered
Lymphadenopathy (Infectious
Mononucleosis)
Characteristics Round, Steinkamp’s L/S ratio <2, large
longitudinal diameters, hyperechoic hilum, sharp borders,
commonly matting or clumping of CLNs, hypervascular,
color/Doppler mode symmetric radial tree-like vascular pattern, low resistance index (RI <0.6).
About 90% or more of adults worldwide are seropositive for
EBV [88]. Infections are more frequent before adolescence,
but EBV can affect patients of all ages. Infection usually proceeds silently, and only 25–30% of cases become clinically
apparent [88–90]. In those patients, a triad of moderate to high
fever, pharyngitis, and moderately tender CLNs with splenomegaly (>50%) characterizes the course of the disease.
Cytomegalovirus, toxoplasmosis, HIV, and human herpes virus
type 1 infections elicit the same symptoms, so these diseases
must be distinguished from infectious mononucleosis.
Plain grayscale ultrasonography In pediatric patients
with acute infectious mononucleosis, 100% of CLNs show a
wide, hyperechoic hilum and have sharp borders (Fig.5.20)
[3]. Hypoechoic foci can occasionally be observed within
the hyperechoic hilum; this might be attributed to the development of germinal follicles in the pulp [91]. Additionally,
matting or clumping of CLNs is common in these patients
and is considered to be the result of periadenitis and adjacent
soft tissue edema (Fig.5.21) [3, 79, 87, 92].
In comparison to reactive lymphadenitis, the EBVinfected CLNs are considerably larger, round, and hypervascular (Fig.5.21) [91]. Vassalo etal. mentioned that L/S≥2 is
a stronger criterion for benign conditions than L/S <2 for
malignancy [93]. Papakonstantinou etal. [3] found that the
majority of the acutely enlarged lymph nodes of infectious
mononucleosis and bacterial lymphadenitis had L/S<2, as
did the lymph nodes affected by malignant lymphoma. In
contrast, the vast majority of hyperplastic lymph nodes
exhibited L/S≥2, but their size was considerably smaller.
Therefore, round shape seems to be a function of size and
rapid growth rather than of internal destruction of the node
[3, 87, 92].
Doppler ultrasonographic assessment of intranodal
vascular resistance
Doppler US shows a central radial
tree- like pattern of vessels in 75% of EBV-infected CLNs;
the other 25% elicit a central hilar vessel (Fig.5.22). This
difference is statistically signicant [3]. Spotted, peripheral, or avascular patterns of perfusion were not observed in
any case of infectious mononucleosis or even reactive
hyperplasia. In infective lymphadenopathy, extensive
inammatory changes in the central part of the CLN may
displace normal lymphatic tissue to the periphery, resulting
in huge enlargement and dilatation of subcapsular vessels,
5 Sonography ofLymph Nodes intheNeck
Fig. 5.20 CLNs with an
acute infectious
mononucleosis show a wide
hyperechoic hilum and have
sharp borders
69
Fig. 5.21 EBV-infected CLNs are considerably larger, round, and
hypervascular. Occasionally hypoechoic foci within the hyperechoic
hilum and matting or clumping as the result of periadenitis and adjacent
soft tissue edema may be seen
whereas extension of the inammation into adjacent fat
planes incites enlargement of pericapsular vessels, similar
to metastatic lymphadenopathy [3, 29, 31, 94]. Vascular
densities are controversial. According to the results of
Papakonstantinou etal. [3], benign processes may manifest
with variable vascular density depending on the rate of
growth and the development of necrotic areas, which cause
perfusion defects. Power Doppler may provide more infor-
Fig. 5.22 Doppler ultrasonography shows a central radial tree-like
pattern of vessels in 75% of EBV-infected CLNs, whereas the residual
25% elicit a central hilar vessel
mation about vascular density (Figs.5.23 and 5.24) [95],
but it does not seem to contribute to the nal categorization
of vascular patterns [94].
Color Doppler sonography is an established method for
the noninvasive documentation and quantication of intravascular blood ow. In the study of Baltas et al., the resistance index (RI <0.6) of intranodal hilum vessels in infectious
70
Fig. 5.23 Benign processes
may manifest with variable
vascular density, which can be
investigated by power
Doppler
J. E. Meyer
Fig. 5.24 A magnied view of Fig.5.23
mononucleosis was low, which indicates a benign lesion; this
nding was in accordance with previous investigations [96].
Qualitative/quantitative elastographic assessment No
investigation has yet been done in this research eld.
5.1.5 Suppurative Lymphadenopathy (Abscesses)
Characteristics Fusion, huge conglomerates, inhomoge-
neous, lost echotexture, liquid areas, induration, hyper/
hypoechogenic areas in a salt-and-pepper pattern, color/
Doppler mode high vascularization, contrast media accumu-
lation, unsharp borders, nodal matting or clumping, adjacent
soft tissue edema.
Plain grayscale ultrasonography
The two kinds of
abscesses—“cold” and “hot”—can be distinguished. Cold
abscesses are more like a suppurative lymphadenopathy; the
fulminant inammation associated with a hot abscess is lacking. Therefore the sonographic characteristics of cold abscesses
are quite similar to those of a necrotic CLN.In contrast, hot
abscesses are the result of a severe infection, which usually also
involves the surrounding connective tissue. Patients with hot
abscesses are very often in bad general condition (high fever;
swollen, reddish neck; pain). Thus, there are two main differential diagnoses: the tuberculosis stage IV/V and malignant,
necrotic CLN disease with accompanying infection [97].
In both cases the abscess is predominantly hypoechoic or
anechoic with a posterior acoustic enhancement. Moreover,
destruction of the internal anatomy of the lymph node or nodes
leads to loss of the hilar structure and vasculature. Occasionally,
an area of suppuration with residual tissue is either hyperechoic
or isoechoic relative to the surrounding tissue [98]. Cold
abscesses usually have more sharp borders (Fig.5.25) than hot
abscesses (Fig.5.26) [99–101]. Moreover, the periadenitis subsequently results in unsharp borders on US imaging, spreads
into subcutaneous tissues with adjacent soft tissue edema, and
shows nodal matting or clumping in the neck [17]. Intranodal
necrosis or huge necrotic areas in CLN conglomerates also can
be visible. Regardless of the nodal size, all lymph nodes with
intranodal necrosis are considered pathologic [102].
On US, the abscess may appear in the beginning as a cystic area within a lymph node. Cystic necrosis appears as an
5 Sonography ofLymph Nodes intheNeck
Fig. 5.25 Cold abscesses
usually are more sharp-shaped
with a predominantly
hypoechoic or anechoic center
71
Fig. 5.26 Hot abscesses tend to be less sharp- or duller-shaped, with a
predominantly hypoechoic or anechoic center and a posterior acoustic
enhancement. Occasionally, an area of suppression with residual tissue
is either hyperechoic or isoechoic relative to the surrounding tissue. No
Doppler sonographic signs elicit loss of solid CLN tissue
echolucent area within the lymph node, with dorsal acoustic
shadowing, whereas in huge conglomerates, echolucent
areas change, with echogenic areas following a salt-andpepper pattern [13, 103].
As a function of the grade of cellulitis and the size of the
abscess, a mass effect with suppression of surrounding tissues occurs [104, 105]. Furthermore, to determine liquefaction within the lymph node, dynamic sonopalpation can be
used. Briey, a uctuation and a compression of the liquid
are induced by gentle, repetitive pressure with the transducer
or the nger over the area of cellulitis. Thus, these simple
maneuvers can demonstrate the presence and extent of liquefaction in an abscess.
Qualitative/quantitative elastographic assessment
Elastography cannot yield any advantages for the diagnosis of a
neck abscess, because abscesses display variable stiffness
according to uid content [106]. On the other hand, elastography visualizes induration of surrounding supercial skin
abscesses. Thereby, asymmetry of abscess induration is associated with failure of standard therapy [107].
Ultrasound-guided ne-needle aspiration (USFNA) and
ultrasound-guided core biopsy (USCB) Aspiration of pus
is helpful for conrmation of suspected diagnosis and for
antibiotic resistance testing at a microbiologic lab.
Occassionally this might also be a therapeutic option.
5.1.6 Lymph Node Metastases ofHead
andNeck Squamous Cell Carcinoma
(HNSCC)
Characteristics Round, inhomogenous or homogenous,
absence of hilum structure, enlarged cortex, longitudinal
diameter >18 mm, minimal cross-sectional diameter>8–10mm, color/Doppler mode peripheral vascularization; Steinkamp/Solbiati index <2.
Plane grayscale ultrasonography The published studies
have not achieved accord in regard to the best ultrasound criteria to indicate a lymph node metastasis of HNSCC.Nevertheless
72
Fig. 5.27 A heterogeneous
texture of a lymph node is
considered as a sign of
malignant transformation and
can be found in more than
90.9% of all metastatic and
only 11.8% of all reactive
cervical lymph nodes
J. E. Meyer
most authors agree that sonomorphologic criteria have a low
sensitivity but a high specicity for differentiating metastatic
from nonmetastatic lymph nodes [14, 15].
In the past, quantitative and sonomorphologic criteria
were separately investigated [13, 16, 108, 109].
Heterogeneous texture of a lymph node was considered as a
sign of malignant transformation [15, 110]. Hessling and
coworkers found a heterogeneous echogenic structure in
90.9% of all metastatic cervical lymph nodes and only 11.8%
of reactive CLNs (Fig.5.27) [110]. In this study, the sensitiv-
ity of echogenic structure was just 23.5%, with a specicity
of 76.5%, which is in accordance with the literature. In contrast, the groups led by Ahuja and Som concluded that metastases have a hypoechogenic structure and look more
homogenous (Fig. 5.28) [17, 19, 102]. Therefore, echogenicity is not a signicant criterion for diagnosing and conrming a lymph node metastasis; it is just one part of the
puzzle. Nevertheless, the appearance of irregular borders
points toward extracapsular spread (ECS) and therefore is a
safe sign of malignancy (Video 5.4).
The appearance of an echogenic hilum in a cervical lymph
node is a sign of a benign condition. Solbiati reported that only
4% of the investigated cervical lymph node metastases had a
hilum [19], and studies by Rubaltelli and Vassallo showed that
84–92% of all benign lymph nodes were an echogenic lymph
node with a hilum [13, 16]. In the study by Meyer etal., 96.5%
of all benign cervical lymph nodes had a hilum, but also 91.5%
of all metastases had a hilum [1]. This gives evidence that the
Fig. 5.28 Until now, echogenicity in HNSCC metastases can be
hyperechogenic and heterogeneous as well as also hypoechogenic and
more homogenous as in this gure. As a result, echogenicity is not a
signicant criterion for diagnosing and conrming a lymph node
metastasis
qualitative criterion “hilum” might only give additional hints
for the exact diagnosis of malignant transformation.
Quantitative parameters moved signicantly into the
foreground. In various studies, the longitudinal, cross-sectional, and minimal transverse diameters have been recommended for the assessment of the diagnosis [16–18, 108,
109]. In publications so far, the suggested longitudinal
diameter of neck metastasis ranges from 5 to 15mm [1, 14,
18, 102, 108, 109]; most of these reports have involved
5 Sonography ofLymph Nodes intheNeck
Fig. 5.29 In a larger cohort
study, interpretation of the
ROC curve suggested 18mm
to be a good cutoff value for
the longitudinal diameter to
distinguish metastatic from
nonmetastatic cervical lymph
nodes. To raise a higher
sensitivity and specicity in
an obviously metastatic neck,
longitudinal diameters of
suspected nodes should
exceed 15–18mm in length,
whereas in clinically
unsuspicious necks, the cutoff
line should be lower, above
10mm in length, to assume
metastatic disease
73
small study cohorts. In a larger cohort study, interpretation
of the ROC curve suggested 18mm to be a good cutoff
value to distinguish metastatic from nonmetastatic CLNs
(Fig.5.29). Sensitivity was 60.5%, whereas specicity was
74.3% [1]. In contrast, the group around Steinkamp proved
the hypothesis that CLNs with a maximal longitudinal
diameter above 10mm could be considered as metastasis;
they reported a sensitivity of 88% but a rather low specicity of 60% [111]. In an obviously metastatic neck, longitudinal diameters of suspected nodes should exceed
15–18 mm, whereas in clinically unsuspicious necks, the
cutoff line to assume metastatic disease should be lower,
>10mm in length. In this way, the sensitivity is higher in a
diagnostic situation with no clinically relevant neck disease,
and specicity increases in a metastatic-neck.
Moreover, this shows that the use of multiple parameters
will be most successful. More recent studies have investigated the minimal diameter of lymph nodes and found that
minimal diameters exceeding 5–10mm are suspect for the
detection of lymph node metastases [13, 108, 112]. Most
authors recommended 8mm as the best cutoff value for the
minimal diameter (Fig.5.30) [1, 14].
Another interesting issue is the calculation of ratios of
diameters to image two-dimensional forms of the lymph
node. The workgroup of Vassallo presented a sensitivity of
85% and a specicity of 86% for the criterion “ratio of longitudinal to transverse diameter” [16]. When Steinkamp and
coworkers applied this ratio, they improved their diagnostic
accuracy from 52% to 93%, compared with the exclusive
observation of the diameters of the lymph nodes [111]. It is
commonly agreed that round-shaped lymph nodes are highly
suspicious for malignancy, and oval-shaped nodes represent
benign ndings [15, 17–20]. On the other hand, a malignant
lymph node at an early stage of conversion can still be oval
[18], and round-shaped lymph nodes are the typical sonographic nding in Hodgkin’s and non-Hodgkin’s lymphoma
[17, 19]. Considering a Steinkamp/Solbiati index of 0.67 to
be the cutoff for round or oval-shaped lymph nodes, data
showed a sensitivity of 64.5%, a specicity of 57.6%, and a
predictor quality of 61.3% for lymph node metastasis
(Fig.5.31).
Along with the discussion of derived quantitative
sonomorphologic criteria, the criterion “volume of lymph
nodes” came into force and raised increased attention,
because an enlargement of a lymph node in general is
considered suspicious for malignancy [16, 17, 113], especially in cases of HNSCC [18]. On the other hand, reactive or
resorptive inammation may also lead to lymph node
enlargement [19, 111], and more importantly, micrometastases smaller than 3mm could not be detected by ultrasound
technique [16, 17, 114]. By using the volume formula for
ellipsoid objects, the possibility that a lymph node is malignant is doubled if its volume is >9mm3 in a patient with
conrmed cancer in the head and neck area. This correlation
is statistically highly signicant (p<0.001) (Fig.5.32).
The use of single sonomorphologic aspects is denitively
less valuable than the combination of multiple criteria. To simplify judgment of the different parameters and bring them
74
Fig. 5.30 Only
determination of multiple
diameters will be most
successful. In more recent
studies a minimal diameter
exceeding 5–10mm are
suspect for the detection of
lymph node metastases,
recommending 8mm as the
best cutoff value
J. E. Meyer
Fig. 5.31 Another interesting
issue is the calculation of a
Steinkamp/Solibiaty index
“ratio of longitudinal to
transverse diameter.” A ratio
of 0.67 is a good value for the
cutoff between round- or
oval-shaped lymph nodes and
a predictor for lymph node
metastasis
together, a statistically proven point scale system was recently
published [1]. After multivariate analysis, it turned out that the
three diameters (longitudinal, transverse, and minimal diameter) and dependent values were the most signicant parameters to distinguish between reactive and malignant lymph
nodes. The ve values were adjusted to 100 points, each under
30 points (Table5.6). As soon as two values turn positive, a
critical sum of 30 points is exceeded, and malignant transformation is very probable, with a sensitivity of 82% and a specicity of 58%; these are comparable to the various published
data for ultrasound in the literature, which have shown 78–98%
sensitivity and 32–100% specicity [14, 108, 111].
5 Sonography ofLymph Nodes intheNeck
Fig. 5.32 Along with the
discussion of derived
quantitative sonomorphologic
criteria, the criterion “volume
of lymph nodes” came into
force and raised increased
attention. By applying the
volume formula for ellipsoid
objects, the possibility of a
potential malignant lymph
node is doubled in a volume
above 9mm
conrmed cancer disease in
the head and neck area
3
in case of a
75
Table 5.6 Point scale of quantitative ultrasound values
Points If
25 Volume > 6cm
23 Longitudinal to transverse diameter > 0.7
22 Longitudinal diameter > 19mm
17 Minimal diameter > 11mm
13 Minimal to maximal transverse diameter > 0.7
100 If the total score is 30 points or more, a
malignant transformation is very proable.
a
Each value was adjusted in the order of its statistical signicance, so
that sum accounts for 100 points. A malignant transformation is very
probable if a critical sum of 30 points is exceeded
3
a
Doppler ultrasonographic assessment of intranodal vascular resistance Metastatic lymph nodes usually have a
peripheral or mixed (hilar and peripheral) vascularization
(Video 5.6) [18, 29, 31, 32, 34, 35, 115]. The presence of
peripheral vascularization and perfusion in malignant nodes
Fig. 5.33 Because peripheral vascularization is common in malignant
nodes, its presence, regardless of the presence or absence of hilar vessels, is highly suggestive of malignancy
is thought to be related to tumor neoangiogenesis and recruitment of capsular vessels, whereas keratinization and intranodal necrosis often cause diminishing of hilar vessels [18, 29,
31, 35]. Because peripheral vascularization is common in
malignant nodes, its presence, regardless of the presence or
absence of hilar vessels, is highly suggestive of malignancy
(Fig. 5.33). Power Doppler ultrasonographic evaluation of
nodal vascular pattern has been reported to have high sensitivity (83–89%) and specicity (87–100%) for differentiating
metastatic and reactive nodes (Video 5.7) [18, 29, 31, 35].
Power Doppler ultrasonography assessment of cervical
nodes improves diagnostic accuracy, but its use may not be
76
J. E. Meyer
necessary in all cases, because grayscale ultrasonography in
combination with the features discussed above already has a
high sensitivity (95%) and specicity (83%) in differentiating metastatic and nonmetastatic nodes [19]. Power Doppler
ultrasonography is useful in patients in whom grayscale
ultrasonography is equivocal, however.
Contrast-enhanced ultrasound Contrast-enhanced ultrasound (CEUS) facilitates more accurate illustration of nodal
vascularization and provides additional information on
lymph node parenchymal perfusion [116]. Its value in differentiating benign and malignant lymph nodes is controversial, however [116–119]. The value of CEUS in routine
clinical practice is limited because it is expensive, timeconsuming, and does not eliminate the need for ne-needle
aspiration cytology (FNAC).
Ultrasound-guided ne-needle aspiration (USFNA) and
ultrasound-guided core biopsy (USCB) cytology
USFNA
and USCB are both of tremendous importance in the differential diagnosis of malignant cervical lymphadenopathies.
Fine-needle aspiration cytology (FNAC) is well established
in adults and is becoming popular in children [120, 121].
Ultrasound-guided FNAC has been shown to be an accurate
method for evaluating cervical lymphadenopathy, with a
high sensitivity (89–98%), specicity (95–99%), and overall
diagnostic accuracy (95–98%) [122–125]. It has been
reported that ultrasound-guided FNAC correctly stages the
neck nodes in 93% of patients with head and neck malignancy [123] and inuences the indications for therapeutic
and elective treatment [125]. In our experience, ultrasoundguided FNAC is performed to conrm the diagnosis whenever the ultrasonographic ndings are equivocal. The
technique aids in tumor staging and treatment planning
[123–126] and also is useful in postoperative surveillance of
neck nodes [127].
Although ultrasound-guided FNAC is useful in most
cases, surgical excision of the lymph nodes and histology are
usually considered mandatory for bulky and symptomatic
lesions or when cytologic ndings are inconclusive for the
diagnosis [128]. It has been reported that ultrasound-guided
core biopsy (USCB) of neck masses can be performed in
pediatric patients under local anesthesia and that the procedure is well tolerated [129]. USCB therefore avoids unnecessary surgical procedures in this group of patients.
5.1.7 Thyroid Carcinoma Lymph Node
Metastases
Characteristics Indeterminate: absence of a hilum and at
least one of the following signs—round shape, increased
short axis, increased central vascularization. Suspicious: cystic areas, microcalcications, peripheral or diffusely
increased vascularization, hyperechoic tissue looking like
thyroid.
The European Thyroid Association (ETA) and the
American Thyroid Association (ATA) recently published
two essential review papers with guidelines on this issue
[130, 131]. In addition to the workup of the thyroid gland
itself, ultrasound should evaluate the presence or absence of
any suspicious CLN in the central or lateral lymph node levels, though it can be difcult in the deep parapharyngeal and
retropharyngeal lymph node levels. When attempting to
identify malignant thyroid metastases, the level of the CLNs
is of particular importance. Leboulleux etal. reported that
almost half of metastatic CLNs are located in levels III and
IV, and the other half are in level VI [22]. Up to 16% of CLN
metastasis occurs bilaterally, whereas unilateral CLN metastases are most frequently located on the same side as the initial thyroid tumor [132].
Abnormal CLNs in thyroid cancer are classied in two
categories: indeterminate and suspicious [130] (Fig.5.33).
Indeterminate CLNs lack a hilum and show at least one of
the following characteristics:
• Rather round shape
• Increased short axis (≥8 mm in level II and ≥5mm in
levels III and IV)
• Increased central vascularization (Fig.5.34).
In this context, the presence of a hilum and the absence of
vascularization are the weakest ultrasonographical signs for
CLNs in thyroid cancer because a hilum is also present in
normal CLNs in 29–48% and 33–36% of the cases, respectively [133–137].
In contrast, suspicious CLNs demonstrate at least one of
the following characteristics (Fig.5.35) [130, 133–137]:
• Microcalcications
• Partially cystic appearance
• Peripheral or diffusely increased vascularization
• Hyperechoic, thyroid-like tissue
Microcalcications and cystic transformation are especially strong indicators for malignancy, because they do not
occur in normal CLNs. Although their sensitivity is only moderate (5–69% for microcalcications and 10–34% for cystic
transformation), their specicity (93–100% and 91–100%,
respectively) was very good, resulting in a high positive predictive value (PPV) of 88–100% and 77–100%, respectively,
with fair accuracies of 56–72% and 48–65% (Fig. 5.36).
Peripheral vascularization, hyperechogenicity, and round
shape do have moderate sensitivity and specicity (of 40–86%,