Eur. Radiol. 2001) 11: 2411 2424
ULTRASOUND*
DOI 10.1007/s00330-001-1163-7
Luigi Solbiati Ultrasound of thyroid, parathyroid glands
Valeria Osti
and neck lymph nodes
Luca Cova
Massimo Tonolini
Abstract In the past 15 years high- be markedly helpful to speed up the
Published online: 25 October 2001
frequency B-mode sonography and diagnostic process. Fine-needle as-
Springer-Verlag 2001
colour power Doppler have be- piration biopsy FNAB) remains the
come the most important and most most accurate modality for the de-
* Categorical Course ECR 2002
widely employed imaging modali- finitive assessment of thyroid gland
ties for the study of the neck, in par- nodules and of any doubtful case of
ticular for thyroid gland, parathy- nodal disease. In association with
roids and lymph nodes. Sonography clinical findings and serum levels of
allows not only the detection but of- parathormone, FNAB has specifici-
ten also the characterization of the ty close to 100 % for the character-
diseases of these organs, distin- ization of parathyroid adenomas. A
guishing benign from malignant le- combined approach with sonogra-
sions with high sensitivity and speci- phy and FNAB is generally highly
L. Solbiati " V. Osti " L. Cova " ficity, which could be further im- effective.
))
M. Tonolini
proved by the employ of ultrasound
Department of Radiology, General
contrast agents and harmonic imag- Keywords Thyroid gland "
Hospital of Busto Arsizio, Piazzale Solaro,
ing. Although no single sonographic Parathyroid glands " Lymph nodes "
3, 21052 Busto Arsizio VA), Italy
criterion is specific for benign or Ultrasonography " Power Doppler "
E-mail: [e-mail]
malignant nature of the lesions, the Colour Doppler
Phone: [phone]
Fax: [phone] combination of different signs can
palpation due to, for example, physical limitations and
Thyroid gland
surgical scars. The size of the normal thyroid gland var-
In the past 15 years high-frequency B-mode sonography ies according to the morphotype of subjects, reaching
and colour-power Doppler have become the most im- 7 8 cm in length with only 0.7 1.0 cm as thickness in
portant and most widely employed imaging modalities thin subjects, whereas in obese patients the length is
for the study of the thyroid gland. This is due to many usually less than 5 cm, but the normal anteroposterior
reasons: the favourable anatomical location of the diameter can reach 2 cm. Being volumetric studies of
gland, the highest degree of vascularity both macro- thyroid lobes easily performable only with 3D ultra-
and microvascularization detectable with colour Dop- sound not yet widely available), thus far thickness is
pler) in normal subjects among all the superficially lo- considered the simplest among the most reliable indexes
cated normal structures of the body and the extremely of thyroid size: when it is larger than 2 cm, enlargement
high incidence of thyroid abnormalities, either nodular can be confidently diagnosed [1, 2, 3].
or diffuse, most of which are benign diseases requiring The normal thyroid parenchyma has a characteristi-
periodical sonographic follow-up. cally homogeneous ultrasound appearance which is
When the thyroid gland is approached with sonogra- more echogenic than the adjacent strap muscle and well
phy, the first relevant parameter to study is the size of distinguishable from the many relevant adjacent struc-
the gland, which is not always easily assessable with tures, i.e. trachea, esophagus, nerves, large blood vessels.
2412
in countries like most southern European countries)
with high prevalence of thyroid goitrous disease sonog-
raphy is capable of detecting small, non-palpable thy-
roid nodules benign in over 90 % of cases) in a large
amount of the population, in order to speed up the di-
agnostic work-up, sonographic criteria have to be em-
ployed to select the suspected lesions to undergo fine-
needle aspiration biopsy FNAB) [7]. On the contrary,
in countries such as those of North America where thy-
roid goiter is generally sporadic, free-hand FNAB is
usually performed as first assessment after the detection
of a palpable thyroid nodule and sonography is per-
formed only when FNAB is not diagnostic or when a
preoperative map of the thyroid gland is needed [8].
Nodular diseases
In the investigation of thyroid nodular diseases, sonog-
raphy has five major applications:
1. Detection of thyroid nodules
2. Differentiation of hyperplasia/goiter from all other
thyroid nodular diseases
3. Preoperative determination of the extent of known
thyroid malignancy
4. Detection of residual, recurrent or metastatic carci-
noma
5. Guidance to FNAB for non-palpable nodules
Fig. 1 a, b Multinodularity does not exclude malignancy. a Multi- As for detection and characterization, each thyroid
ple nodules with different echogenicity isoechoic, mixed, cystic
nodule has to be studied paying attention to its level of
with dense fluid) in benign goiter. b Two contiguous hypoechoic
echogenicity compared with the normal parenchyma,
nodules with microcalcifications and irregular margins: multifocal
the presence of calcifications or cystic changes, the pat-
papillary carcinoma
tern of margins, the presence of peripheral echo-poor
ªhaloº and the amount and distribution of blood supply
[3, 9, 10, 11].
Thyroid pathologies are classifiable into two groups, Hyperplasia is the most common pathology of thy-
nodular and diffuse diseases. roid gland, accounting for 80 85 % of all thyroid nod-
All thyroid diffuse diseases with the exception of the ules, and is more common in women [12]. It may be fa-
extremely rare diffuse primary lymphoma) and approx- milial, due to iodine deficiency, to compensatory hyper-
imately 90 92 % of nodular pathologies are benign [4]. trophy or secondary to hypoplasia of one lobe or partial
Actually, thyroid cancer is rare, accounting for less than thyroidectomy. When single or multiple hyperplastic
1 % of all malignant neoplasms [5]. Sonography is sig- nodules lead to a global enlargement of the gland, the
nificantly more sensitive than clinical palpation in iden- term goiter either single or multinodular) is properly
tifying thyroid nodules [6] and in detecting multinodu- used. Patients with hyperplasia/goiter are frequently
larity when single nodules are clinically diagnosed. asymptomatic but may occasionally present with com-
Studies comparing clinical palpation with thyroid imag- pressive symptoms or rapidly enlarging mass, usually
ing show a prevalence of 13 50 % for the detection of indicating spontaneous haemorrhagic changes within
thyroid incidentalomas [7, 8]. In recent years, high-res- the nodule s). Hyperplasia may have a diffuse or nodu-
olution sonography has confirmed the pathological lar pattern. Diffuse hyperplasia results in the enlarge-
statement that multinodularity does not necessarily ment of one or both lobes, with lateral or posterior de-
mean benign disease or does not exclude malignancy viation of the great vessels and/or the trachea, but never
Fig. 1) [4, 6], being the rare thyroid malignancies often with infiltration of their walls. Mono- or multinodular
found in association with one or more benign nodules, hyperplasia is usually seen as single or multiple discrete
both in the same and in the opposite thyroid lobe. Since nodules, varying greatly in number and size, separated
2413
2a 2b
2d
2c
3
Fig. 2a d Four different examples of thyroid nodular hyperplasias
by normal parenchyma. They are mostly isoechoic
with typical features of benign nature: a isoechoic with thin regular
Fig. 2) and hyperechoic with well-defined margins. The
halo and small internal cystic change, b isoechoic with peripheral
very unusual hypoechoic nodular hyperplasias 5%) are
vascularity and wide internal fluid-filled area, c cystic with multiple
due to ªsponge-likeº multilocular lesions filled with
comet-tail artefacts due to colloid substance and d isoechoic,
colloid substance. Cystic changes are present in 60 70 %
markedly hypovascular within a highly vascularized thyroid pa-
renchyma of cases, due to either haemorrhages Fig. 2) or colloid
substance collections: in this latter circumstance, typical
Fig. 3 Thyroid adenoma with characteristic arrangement of the
comet tail artefacts are seen within the nodules Fig. 2).
blood supply: peripheral vascularity with ªspoke-and-wheelº ap-
pearance of the blood vessels towards the centre of the mass Macro-calcifications are present in 20 25 % of goitrous
nodules, usually with greater incidence in elderly pa-
tients or ªoldº nodules, representing the final patholog-
ical evolution of these lesions. The calcifications of goi-
trous nodules are typically curvilinear, annular or dys-
2414
Fig. 4 Hyperfunctioning thy-
roid nodule seen as a hypervas-
cularized nodule on colour
Doppler and b lesion with high
uptake on isotope scintigraphy
Fig. 5 a, b Papillary carcinoma
with typical features: a hypo-
echogenicity, microcalcifica-
tions and b hypervascularity
with chaotic arrangement
4a 4b
5a 5b
morphic and seen as large, densely calcified areas with ªspoke-and-wheelº arrangement which is clearly visible
posterior shadowing [4]. As clearly demonstrated by with colour Doppler Fig. 4).
pathological studies, hyperplastic goitrous nodules are Hyperfunctioning thyroid nodules may pathological-
usually less vascularized than normal thyroid parenchy- ly be either hyperplastic nodules or adenomas. In this
ma, with the exception of rapidly growing hyperplastic latter circumstance, hypervascularity Fig. 5) and typi-
lesions in young patients. As a consequence, on colour- cal blood supply arrangement allow for a highly reliable
power Doppler these nodules usually appear poorly recognition of the hyperfunctioning lesion within the
vascularized, with prevalent perilesional blood supply thyroid parenchyma, with reported sensitivity of 96 %
Fig. 3). Unfortunately, with the increasing sensitivity to and specificity of 75 % [13].
slow blood flows of modern power-colour Doppler Malignant neoplasms of the thyroid gland are quite
technology, a great amount of hyperplastic/goitrous rare 2 3 cases per 100,000 individuals).
nodules currently show also intralesional flow signals. Papillary carcinoma is the most common malignan-
Therefore, the sign of ªexclusively perilesional blood cy of the thyroid gland 60 70 % of all thyroid malig-
flow signalsº on colour Doppler is markedly decreasing nancies) [14]. It affects women more often than males
its relevance as character of benign nature. and is prevalent in patients under 20 and above
Non-goitrous nodules include mostly adenomas and 70 years of age. Slow growth and good prognosis are
carcinomas. common features of this neoplasm, the reported 20-
Adenomas represent only 5 10 % of all nodular dis- year survival rate being as high as 90 % [15]. On ultra-
eases of the thyroid and are more common in women sound papillary carcinoma appears as a predominantly
[5]. Thyroid adenomas may be either hypoechoic, iso- hypoechoic nodule, mostly solid, even if in 20 30 % of
echoic like most follicular adenomas) or hyperechoic. cases cystic changes with detectable blood supply
Characteristically, they usually show a thick and smooth within intracystic septa may be seen ªcystic-papillary
peripheral echo-poor halo, likely representing fibrous carcinomaº; Fig. 6). Intralesional punctate calcifica-
capsule and peripheral blood supply of the tumour. tions microcalcifications), are characteristically pre-
Even more typically, from the periphery blood vessels sent in 85 90 % of these tumours and are highly reli-
move to the centre of the lesion, with a relatively regular able for the sonographic diagnosis of papillary carci-
2415
appearance of the primary tumour, showing microcal-
cifications, cystic changes or chaotic hypervascularity
Fig. 7).
Follicular carcinomas account for 5 15 % of thyroid
cancers, with higher incidence in older patients [1]. In
most cases they develop from pre-existing adenomas
[16, 20]. Follicular carcinomas are associated with hy-
perplastic/adenomatous thyroid nodules in 60 70 % of
cases. The most significant pathological criteria for the
diagnosis of follicular carcinoma are invasion of the
capsule and vascular invasion. Minimally invasive fol-
licular carcinomas, with capsular infiltration but no
vascular invasion, have a low mortality rate 3 %).
6
Frankly invasive follicular carcinomas, with invasion of
vascular supply and thyroid parenchyma, metastasize in
50 80 % of cases and have high mortality rate 50 %).
Both histotypes spread via the blood to bone, lung,
brain and liver [12].
On ultrasound follicular carcinomas are predomi-
nantly solid, homogeneous, mostly hyperechoic or iso-
echoic Fig. 8). Thick irregular capsule, tortuous peri-
nodular and intranodular blood vessels and signs of ex-
tracapsular spread are sonographic signs suggesting the
diagnosis of malignant lesion Fig. 8) [16]; however,
even FNAB cannot be diagnostic in most cases, being
capsular and vascular invasions signs detectable only
with histology of surgical specimens.
Anaplastic carcinomas represent 5 10 % of all thy-
roid cancers, occur mostly in elderly people and are
highly aggressive, with 5-year mortality rate of more
than 95 % [14]. They typically present as rapidly en-
larging masses extending beyond the gland and invading
adjacent structures. Frequent association with papillary
7
or follicular carcinomas has been reported [1].
Fig. 6 Cystic papillary carcinoma with microcalcifications and With sonography, anaplastic carcinomas are diffusely
blood vessels in the solid portion of the mass
hypoechoic, with areas of necrosis in 78 % of cases,
Fig. 7 Thyroid mass with aspecific sonographic features: iso- dense amorphous calcifications in 58 % and nodal or
echogenicity, no microcalcifications, perilesional and internal
distant metastases in 80 % [7, 21]. Furthermore, even
blood supply. The histological diagnosis is follicular carcinoma
more diagnostically useful, sonographic signs of this
cancer are marked irregularities of the boundaries and
the early invasion of thyroid gland capsule, with infil-
noma or, much more rarely, of medullary carcinoma; tration of adjacent structures Fig. 9).
Fig. 6). With high-frequency ultrasound, they appear Medullary carcinomas account for only 5 % of all
highly echogenic but typically do not exhibit posterior thyroid malignancies. In 20 % of the cases they may be
shadowing. Pathologically, they represent calcified familial, occurring in association with the multiple en-
psammoma bodies, which are a typical landmark of this docrine neoplasia MEN IIA) syndrome. Slow growth
disease. On colour-power Doppler, hypervascularity and spread via the lymphatics to nearby lymph nodes
with chaotic arrangement of blood vessels, related to are characteristic features. Medullary carcinomas are
arteriovenous shunts and tortuosity of vessel course, is multicentric and/or bilateral in approximately 90 % of
commonly seen 90 % of cases; Fig. 6) [15, 16]. The the familial cases. Prognosis is considered to be gener-
major route of spread of papillary carcinoma is through ally worse than that for follicular cancer.
the lymphatics of the neck and therefore laterocervical The sonographic appearance of medullary carcinoma
and/or recurrent adenopathies are either often associ- is similar to that of papillary carcinoma: hypoechoge-
ated with the primary tumour at initial diagnosis ap- nicity, irregular margins, microcalcifications histologi-
proximately 50 % of cases) [17, 18, 19] or may develop cally representing calcified deposits of amyloid), hyper-
after thyroidectomy. These nodes often reproduce the vascularity with irregular arrangement of blood vessels)
2416
89 a 9 b
Fig. 8 Large anaplastic carcinoma with irregular margins, posteri- be assigned to all the most important sonographic signs
or extracapsular growth and infiltration of the laryngeal recurrent
of thyroid nodules. These data are summarized in Ta-
nerve arrow)
ble 1.
Fig. 9 a, b Patient with family history of multiple endocrine neo-
In recent years several papers in the international
plasia II A. a In the left lobe of the thyroid gland, there is a large
literature have reported data concerning the reliability
hypoechoic nodule with thick halo and scattered microcalcifica-
of sonography B-mode and colour/power Doppler) in
tions. Pathological diagnosis: medullary carcinoma. b On the right
the differentiation of benign vs malignant thyroid nod-
side, typical parathyroid adenoma oval, hypoechoic, with regular
ules, employing the sonographic features described
margins) is seen caudally to the thyroid lobe
above. Sensitivity rates ranged from 63 to 87 %, speci-
ficity from 61 to 95 % and overall accuracy from 80 to
94 % [8, 24, 25]. In the near future, contrast-enhanced
and frequent association with metastatic lymphadenop- sonographic studies using microbubbles could further
athies are the most distinctive features [12, 22]. improve the diagnostic capabilities of sonography. Thus
Thyroid primary lymphoma is rare 4 % of all thyroid far, preliminary experiences with the first generation,
malignancies), mostly of the non-Hodgkin's type and galactose-based contrast agent seem to provide useful
usually affects elderly females. The typical sign is a rap- data for the differentiation of benign vs malignant nod-
idly growing mass which may cause symptoms of ob- ules through the analysis of the time-intensity curves
struction such as dyspnea and dysphagia. In 70 80 % of correlating the variation of signal intensities during the
cases, thyroid lymphoma arises from a pre-existing contrast transit time [26].
chronic thyroiditis with subclinical or overt hypothy- Even though no sonographic feature is pathogno-
roidism [23]. Prognosis is highly variable and depends monic for malignancy, the high rates of sensitivity and
on the stage of the disease. The 5-year survival rate may specificity reported account for the current major role
range from nearly 90 % in early-stage cases to less than of sonography among all imaging modalities in thyroid
5 % in advanced, disseminated disease. nodular lesions. Its use is likely to be complementary,
Sonographically, thyroid lymphoma appears as a hy- rather than alternative, to FNAB which is the most ef-
poechoic, lobulated, nearly avascular mass. Large areas fective method for diagnosing malignancy in a thyroid
of cystic necrosis may occur, as well as encasement of nodule. The FNAB is reported to have sensitivity ranges
large blood vessels of the neck. The adjacent thyroid of 65 98 % specificity of 72 100 %, false-negative rates
parenchyma may be heterogeneous due to associated of 1 11 % and false-positive rates of 1 8 % [27, 28].
chronic thyroiditis [23]. In our opinion, in patients presenting with one or
Once a thyroid nodule has been detected with more palpable thyroid nodules, the initial imaging mo-
sonography the fundamental problem is to determine dality to be performed should be chosen on the basis of
whether it is benign or malignant. For this purpose, all laboratory tests: if the blood levels of TSH are either
the different sonographic signs described above echo- normal or increased, sonography including colour/
genicity, margins, peripheral halo, amount and ar- power Doppler) has to be the first imaging test. If no
rangement of vascularity, microcalcifications, invasion sonographic signs suggesting malignancy are detected
of adjacent structures) have to be singularly analysed and no clinical data of possible malignancy e.g. rapid
and combined with clinical data in order to differenti- growth, hard consistency, history of neck radiotherapy
ate purely benign nodules from lesions requiring cyto- treatment) are reported, no further assessment is need-
logical assessment by FNAB, being suspected of ma- ed and only a 6- to 12-month sonographic follow-up
lignancy. study is advisable. If even a low probability of malig-
According to our experience and the literature, nancy is sonographically suspected, FNAB is the man-
rates of likelihood of benign or malignant nature can datory further assessment. On the contrary, if TSH lev-
2417
Table 1 Likelihood of benign or malignant nature assigned to the
most important sonographic signs of thyroid nodules. Modified
from [3])
Feature Benign Malignant
Internal contents
Purely cystic content ++++ 
Cystic with thin septa ++++ +
Mixed solid and cystic +++ ++
Comet-tail artefact ++++ +
Echogenicity
Hyperechoic ++++ +
Isoechoic +++ ++
Hypoechoic ++ +++
Halo
Thin regular halo ++++ ++
Thick irregular halo ++ +++
Margin
Fig. 10 Graves-Basedow disease with peak systolic velocities of
Well defined +++ ++
approximately 85 cm/s
Poorly defined + +++
Calcification
Eggshell calcifications ++++ +
Coarse calcifications +++ +
In conclusion, a combined approach with sonography
Microcalcifications + ++++
and FNA in patients with questionable thyroid nodules
Doppler
is generally highly effective. In fact, the extremely low
Peripheral flow pattern +++ +
probability to develop thyroid malignancies during a 6-
Internal flow pattern ++ +++
year follow-up period in patients with benign FNA has
+ rare probability < 1 %); ++ low probability < 15 %); +++ inter- been already reported. Consequently, the possibility of
mediate probability 16 84 %); ++++ high probability > 85 %)
missing a malignancy in a patient in whom both sonog-
raphy and FNAB do not yield malignant features is ac-
tually very small [29].
els are increased, with a reasonable likelihood of thyroid
hyperfunction, isotope scintigraphy has to be the initial
imaging test, with the essential aim of differentiating Diffuse diseases
between diffusely hyperfunctioning thyroid gland and
ªhotº nodules. Several thyroid diseases are characterized by diffuse
As for the increasingly frequent issue of nonpalpable rather than focal involvement: acute suppurative thy-
nodules incidentally detected by sonography, three dif- roiditis; subacute granulomatous or De Quervain's thy-
ferent criteria even though with possible overlapping in roiditis, and chronic lymphocytic thyroiditis, called
some instances) may be followed in the diagnostic work- Hashimoto' s disease in its goitrous form [35]; colloid
up: diffuse goiter and Graves' disease, the commonest cause
of thyrotoxicosis. Diagnosis of these conditions is usu-
1. Size: according to this parameter, all nodules ex- ally made on the basis of clinical and laboratory findings
ceeding 1.0 cm in maximum diameter should be and, on occasion, by FNAB, with a very limited role of
punctured, irrespective of physical and sonographic sonography.
features, whereas lesions under 1.0 cm should be only In hyperplasia with hyperfunction Graves' disease)
followed on time. the gland contours are lobulated and the size is in-
2. Clinical sonographic features: patients with history creased, with usually prompt response to effective
of neck irradiation or familial history of MEN dis- medical treatment: size reduction is a useful indicator of
ease and patients presenting with cervical adenopa- therapeutic success. The echotexture may be more in-
thies with sonographic appearance consistent with homogeneous than in diffuse goiter, mainly because of
malignancy and thyroid nodule s) of any size must the presence of numerous large intraparenchymal ves-
undergo ultrasound-guided FNAB of both thyroid sels. Furthermore, especially in young patients, the pa-
nodule s) and adenopathies. renchyma may be diffusely hypoechoic either due to the
3. Purely sonographic features: nonpalpable nodules extensive lymphocytic infiltration or to the predomi-
showing sonographic features highly suspected for nantly cellular content of the parenchyma, almost lack-
malignancy should always undergo ultrasound-guid- ing of colloid substance. Colour flow Doppler and
ed FNAB [5]. spectrum analysis confirm the hypervascular pattern
2418
progressive functional normalization. In the majority of
cases subacute thyroiditis responds well to medical
therapy with complete recovery of thyroid function
within a few weeks. Histologically, interstitial oedema
and cellular exudation with destruction of follicular cells
are the predominant phenomena.
Although subacute thyroiditis is easily diagnosed
clinically, sonographic findings are pathognomonic [31].
In the initial stage the affected segments of the thyroid
appear enlarged, with ill-defined, irregular margins and
markedly hypoechoic structure with high acoustic ab-
sorption. With colour Doppler vascularization appears
normal or, more commonly, reduced owing to the dif-
fuse oedema of the gland. As the disease evolves, re-
covery of the normal thyroid structure may take pseud-
onodular form, involving asynchronously the various
pathological foci. Occasionally, hypoechoic areas in-
crease in size on follow-up examinations, requiring fur-
ther medical treatment; therefore, the main roles of
sonography in subacute thyroiditis are to assess the
evolution of the disease and the timing of medical ther-
apy and to detect early possible recurrences.
Chronic autoimmune thyroiditis is more frequent in
women 9:1) and in patients with other autoimmune
pathologies. Thyrotoxicosis may be the initial clinical
Fig. 11 a, b Chronic lymphocytic thyroiditis. a Severe disease, with presentation, related to excessive hormonal release
pseudolobules, fibrous septa, irregular margins and very low level
stimulated by antibodies hashitoxicosis). Following this
of echoes. b Occult disease with hypoechoic micronodules and
phase, hypothyroidism slowly develops, together with
mild irregularities of margins
the progression of histological changes, consisting of
lymphocytic infiltration and fibrosis.
The typical sonographic features are increase in size,
that Ralls called ªthyroid infernoº: intrathyroid arteries lobulated margins, fibrotic septa ªpseudolobulatedº
present turbulent blood flow with arterovenous shunts appearance) [32] and particularly ªmicronodulationº
and the highest peak systolic velocities found in thyroid [33], namely the dissemination in the whole thyroid pa-
diseases 50 120 cm/s), due to a flow rate usually ex- renchyma of hypoechoic rounded spots, commonly
ceeding 70 cm/s Fig. 10). 1 6.5 mm in size Fig. 11). Histologically, they represent
There are at present no demonstrations of correla- lobules of thyroid parenchyma with massive infiltration
tion among degree of thyroid hyperfunction assessed on of lymphocytes and plasma cells, surrounded by a hy-
the laboratory parameters, extent of hypervasculariza- perechoic ring of fibrous strands. Micronodulation is a
tion and flow-velocity values. On the contrary, in highly sensitive sign of chronic thyroiditis, with a posi-
Graves' disease it has been demonstrated that the fea- tive predictive value of 94.7 % [33].
tures of hypoechoic thyroid parenchyma and high flow With colour Doppler marked intraparenchymal hy-
in the thyroid artery and glandular parenchyma prior to pervascularity, chiefly arterial, is mostly detected, espe-
starting medical therapy are highly specific for the pre- cially inside the hyperechoic septa. This pattern does
diction of relapse of hyperthyroidism at the end of the not differ significantly from the ªthyroid infernoº de-
treatment [30]. In the course of medical treatment of scribed in Graves' disease, but in chronic thyroiditis
Graves' disease, a significant decrease in flow velocities blood flow velocities mostly remain within normal lim-
of the inferior and superior thyroid arteries is usually its, both before and following medical treatment.
recorded. It is generally directly proportional to the de- The end stage of chronic thyroiditis is the atrophic
crease of the free fractions of thyroid hormones. form: the thyroid gland is small, with ill-defined margins
Subacute granulomatous or De Quervain's) thy- and heterogeneous texture due to progressive increase
roiditis is a self-limiting viral disease, usually preceded of fibrosis. Blood flow signals are completely absent.
by infection of the upper airways. In the initial stage, A quite peculiar, though not exceptional, finding is
transient hyperthyroidism due to massive follicular the coexistence of thyroid nodules, benign or malignant,
rupture has been reported. Subsequently, moderate and with chronic lymphocytic thyroiditis. Cytology is often
transient hypothyroidism may occur, related to slowly needed to achieve the final diagnosis [34].
2419
12 a 12 b
1
2
a
1
2
b
13
14 a
14 b
Fig. 12a, b Parathyroid hyperplasias in secondary hyperparathy- In summary, sonography plays a minor role in the
roidism. a Transverse scan of the thyroid gland: large hypoechoic
diagnosis and management of diffuse thyroid diseases,
parathyroid hyperplasia on the right side and small lesion on the
although some sonographic features are nearly pathog-
left side. Both lesions are located posteriorly to the thyroid lobes
nomonic of definite diseases. Sonography can be useful
and show peripheral capsule. b Longitudinal scan of the thyroid
in diagnosing subclinical forms of diffuse disease, in de-
lobe with two small, rounded, hypoechoic and capsulated par-
athyroid hyperplasias termining the coexistence of nodular lesions and thy-
roiditis, and in monitoring changes in textural and vas-
Fig. 13 Primary hyperparathyroidism. Large hypervascular par-
cular patterns during medical treatment.
athyroid adenoma with both internal and perilesional blood flow
signals
Fig. 14 a, b Cystic parathyroid tumours. a Highly echogenic par-
athyroid adenoma with wide cystic changes and perilesional blood
Parathyroid glands
flow signals. b Anechoic parathyroid cyst with perilesional blood
supply
Normal parathyroid glands are not detectable with any
imaging modality, due to small size and structural pat-
tern similar to that of the adjacent thyroid parenchyma;
Painless silent) thyroiditis has the typical histologi- however, when there is biochemical evidence of hyper-
cal and sonographic hypoechogenicity, micronodula- parathyroidism HPT), high-frequency sonography is
tion and fibrosis) pattern of chronic autoimmune thy- commonly used to detect abnormal parathyroid glands,
roiditis, but clinical symptoms may be completely ab- being a highly accurate non-invasive procedure for this
sent in most cases Fig. 11). Usually the detection is oc- purpose.
casional during sonographic studies of the neck per- Primary hyperparathyroidism is now recognized as a
formed for different purposes. Slow progression to hy- common endocrine disease, especially in patients over
pothyroidism is a common finding. 50 years old. The three main aetiologies are: adenoma
2420
almost always limited to a single gland); hyperplasia mours; however, the glands may be inconsistently and
which involves all four glands); and carcinoma. Ade- asymmetrically enlarged, and the diagnosis of multiple
noma is the most common cause of HPT 80 % of cases) gland disease often is difficult to make sonographically.
[35]. The preoperative localization of parathyroid tu- The appearance may be misinterpreted as solitary ade-
mour s) is highly recommended, since it allows for a re- nomatous disease, or the diagnosis may be missed alto-
markable shortening of operative time, especially when gether if the glandular enlargement is minimal.
surgery is complicated by, for example, anatomical pe- In most cases, parathyroid carcinomas are indistin-
culiarities and abnormal locations of the glands. In ad- guishable sonographically from large benign adenomas.
dition, preoperative localization reduces the risk of Gross evidence of invasion of adjacent structures, such
damaging the laryngeal nerve and normal parathyroids as vessels or muscles, is the only reliable preoperative
[4, 36, 37]. sonographic criterion for diagnosis of malignancy, but
Secondary hyperparathyroidism is usually a response this is an uncommon finding Fig. 14) [1, 4]. Further-
to chronic hypocalcaemia in uraemic patients. Since more, benign lesions are mobile when patient swallows,
surgery is advisable only in advanced cases, ultrasound whereas malignant lesions may be fixed [35].
examination may help the clinical management of these Parathyroid glands have an extreme variability of
patients, monitoring size and structure changes during number and location in normal subjects. Most subjects
medical treatment, but may also help the surgical man- have four glands which are located posteriorly to the
agement, facilitating the detection of enlarged supernu- upper and lower poles of the thyroid gland; however, in
merary parathyroid glands or glands in atypical posi- as many as 25 % of normal subjects more than four
tions [38]. glands are present [39, 40].
Parathyroid adenomas and hyperplasias have usually When parathyroid tumours are ectopically located,
oval or oblong shape, with longitudinal diameter rang- the sonographic detection may be more difficult: intra-
ing from 7 to 15 mm. The smallest adenomas can be thyroidal glands 1 % of cases) mimic thyroid nodules,
minimally enlarged glands that appear virtually normal being hypoechoic with well-defined margins. Retro-
during surgery but are found to be hypercellular on tracheal glands are hardly detectable because of the
pathological examination Occasionally, the largest ade- acoustic shadowing from the trachea. Finally, the unde-
nomas may have tubular shape and exceed 4 5 cm in scended glands, situated along the course of the com-
longitudinal size. They are mostly homogeneously solid, mon carotid artery or the recurrent laryngeal nerve, are
markedly more hypoechoic than the adjacent thyroid similar to laterocervical lymph nodes [35].
tissue. This characteristic hypoechogenicity is due to the False-positive sonographic diagnoses may be due to
uniform hypercellularity of the gland, which leaves few prominent blood vessels, oesophagus, longus colli mus-
interfaces for reflecting sound. Parathyroid lesions are cle, thyroid nodules and enlarged cervical lymph nodes,
separated from thyroid tissue by an echogenic plane, whereas false-negative results are caused by minimally
representing the capsule [35]. Most adenomas and hy- enlarged adenomas, adenomas obscured by enlarged
perplasias are hypervascular on colour Doppler, with thyroid goiters, and ectopic adenomas.
prominent diastolic flow Fig. 12). The sensitivity of ultrasound for the parathyroid ad-
In 15 20 % there are variations in the echotexture of enoma localization in primary HPT ranges between 70
parathyroid tumours. and 80 % [1, 41, 42, 43]. Specificity may be improved
Occasionally, the level of echogenicity can be similar with ultrasound using FNAB. Sonography also permits
to that of thyroid parenchyma, increasing the difficulties the reliable differentiation of parathyroid adenomas
for the sonographic differential diagnosis; approxi- from other pathological structures such as thyroid nod-
mately 2 % have internal cystic components that are due ules or cervical lymph nodes [44, 45, 46]. In persistent or
to cystic degeneration Fig. 13). More rarely, purely recurrent hyperparathyroidism, the reported sensitivity
cystic adenomas may be found Fig. 13). Solitary par- of ultrasound ranges between 36 and 63 % [43, 44]. Ul-
athyroid cyst, more frequent in women, occur below the trasound augmented by FNAB and PTH assay can lead
level of the inferior thyroid margin in 95 % of cases; to a specificity approaching 100 % [47, 48].
65 % of them involve the inferior parathyroid glands. In conclusion, pre-operative localization of the par-
The cystic fluid has high levels of parahormone. Calci- athyroid glands is useful for the following purposes:
fications are rare in adenomas and more common in
carcinomas and hyperplasias due to secondary HPT, 1. To identify one abnormal parathyroid gland: this al-
because of the long duration of these diseases. lows for unilateral neck exploration, thus reducing
Preoperative serum calcium levels are usually higher operative time and surgical complications.
in patients with larger adenomas. When multiple par- 2. To localize parathyroid tumours in post-operative
athyroid tumours either adenomas or hyperplasias) are either persistent or recurrent HPT: the complication
present in the same patient, they have the same sono- rate at re-operation is relatively high and the success
graphic and gross appearance as single parathyroid tu- rate decreased [36, 46].
2421
Fig. 15 Parathyroid carcinoma with non-specific sonographic fea- Fig. 16 Schematic representation of cervical lymph nodes grouped
tures: mild hypoechogenicity and irregular margins in six levels. Level VII is located in the upper mediastinum
3. In case of negative results with ultrasound, to aid in extracapsular spread; characteristics of vascularity; and
the differential diagnosis of hypercalcaemia which calcifications.
can be related to causes other than HPT. Normal lymph nodes are formed by an outer cortex
with lymphoid follicles and an inner medulla with lym-
phatic sinuses, connective tissue and blood vessels.
Reactive nodes are sonographically indistinguishable
Neck lymph nodes
from normal nodes. Most inflammatory diseases, except
In the normal adult neck there may be up to 300 lymph for granulomatous infections such as tuberculosis, in-
nodes, ranging in size from 3 mm to 3 cm. Lymph nodes volve lymph nodes diffusely and homogeneously, gen-
are small, oval or reniform bodies lying along the course erally preserving their normal oval shape Fig. 16). On
of lymphatic vessels. When a node undergoes antigenic the contrary, the neoplastic infiltration of lymph nodes
stimulation, it reacts with an increase in size and vascu- occurs primarily in the cortex; therefore, malignant
larity [4]. Many pathologies of the head and neck region nodes tend to have a greater transverse diameter, with a
present as palpable lymph nodes, most of which are su- rounded, asymmetrical morphology of the node
perficially located. Using high-frequency ultrasound, Fig. 16). The long-to-short-axis ratio L/S ratio) can
multiple nodes in all areas of the neck can be detected be employed for the distinction between benign
and their morphology and vascularity can be thoroughly L/S > 2.0) and malignant nodes L/S < 2.0) [52, 53, 54,
assessed; however, due to the different echotexture and 55, 56].
size, it is more difficult to detect benign innocent than The centrally located, thick and regular echogenic
malignant lymph nodes. hilum is a common feature of normal lymph nodes.
Neck lymph nodes can be classified according to Malignant nodes have thin hilum, because of the pe-
their anatomical location: submental; submandibular; ripheral neoplastic infiltration: often the hilum is ec-
parotid; facial; deep cervical; spinal accessory; trans- centric or completely lacking), with associated eccen-
verse cervical; retropharyngeal; occipital; and mastoid tric cortical widening Fig. 17) [56].
[4, 49, 50]. A further topographic classification, per- As for the echotexture of the cortex, lymphomatous
formed by AJCC [51], is based on 7 ªlevelsº, usually nodes have thickened, uniformly hypoechoic cortex,
employed in order to plan surgical interventions. Lev- whereas metastatic nodes show a more echogenic and
el I includes submental and submandibolar nodes; heterogeneous cortex. In patients with known primary
levels II, III and IV include deep cervical chain, the cancer, the presence of necrosis in a lymph node is a
nodes deep to the sternocleidomastoid muscle and the highly probable sign of malignancy: it may appear as a
upper spinal accessory chain. Level V includes the true cystic area or a hyperechoic zone coagulative ne-
transverse cervical chain; level VI the anterior cervical crosis; Fig. 18). Cystic necrosis is also often identified in
nodes and level VII nodes in the superior mediasti- tuberculous nodes, commonly located in the spinal ac-
num Fig. 15). cessory chain and in the supraclavicular region. They
Once lymph nodes are detected, it is mandatory to tend to be clumped together, with associated inflamed
define whether they are benign or malignant. For this surrounding interstitium [56]. Whenever cystic necrosis
purpose, eight parameters should be evaluated: size; is detected in a node, aspiration biopsies for both cytol-
shape; echogenic hilum; level of echogenicity; necrosis; ogy and microbiology studies should be performed.
2422
Fig. 17 a, b Hyperplastic lymph
node of the neck with elongat-
ed shape. a Central hilum, and
b central hilar blood supply
Fig. 18 Rounded hypoechoic
adenopathy with eccentric thin
hilum
Fig. 19 Typical metastatic ade-
nopathy: rounded, isoechoic,
with multiple poles of vascular
supply, both perilesional and
intralesional
17 a 17 b
Fig. 20 a Rounded hypoechoic
tuberculous nodes with macro-
calcifications and poor mostly
perilesional) vascular supply.
b Lymphomatous node Hodg-
kin's disease) with poor vascu-
larity. Blood vessels show pre-
dominantly hilar and regular
arrangement
18 19
20 a 20 b
Normal lymph nodes have smooth margins. In ma- vessels mixed capsular hilar vascularity; Fig. 19, 20)
lignant transformation nodes have rounded and well- [59]. The amount of extrahilar vessels is higher in meta-
defined margins. With advancing malignancy, margins static nodes than in lymphomatous nodes, which is likely
become less defined and sharp, due to possible extra- due to different angiogenesis. Malignant nodes have
capsular spread. pulsatility index PI) and resistive index RI) higher
The patterns of vascularity and their changes are than benign nodes; cut-off values are 1.3 for PI and 0.72
very important in distinguishing between benign and for RI [59, 60, 61]. Three-dimensional sonography can
malignant nodes. Histopathological studies have shown be helpful in detecting more easily abnormal vascula-
that arteries and veins enter the node at the hilum and ture, especially subcapsular and intranodal tortuous
spread in bundles which course longitudinally with the vessels [62].
long axis of the node. Capillaries arising from these hilar No single sonographic criterion is absolutely specific
and medullary vessels feed the nodal cortex [57, 58]. for benign or malignant nature; however, rounded
Hilar flow with central vascular pattern is seen in most shape, absence of hilum, irregular or spiculated outline,
98 %) benign nodes. On the contrary, most malignant coagulative or cystic necrosis, and chaotic capsular
nodes 78 %) show aberrant vessels with curved course blood flow pattern are signs highly suspicious for ma-
entering from the nodal capsule, in addition to hilar lignancy, especially when they coexist in the same node.
2423
For any doubtful case, the most reliable diagnostic mo- have accuracy of 89 90 %, sensitivity of 76 78 % and
dality is ultrasound-guided FNAB, which is reported to specificity of 98 100 % [4, 63].
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