Thyroid gland
In the past 15 years high-frequency B-mode sonography

and colour-power Doppler have become the most im-

portant and most widely employed imaging modalities

for the study of the thyroid gland. This is due to many

reasons: the favourable anatomical location of the

gland,the highest degree of vascularity (both macro-

and microvascularization detectable with colour Dop-

pler) in normal subjects among all the superficially lo-

cated normal structures of the body and the extremely

high incidence of thyroid abnormalities,either nodular

or diffuse,most of which are benign diseases requiring

periodical sonographic follow-up.

When the thyroid gland is approached with sonogra-

phy,the first relevant parameter to study is the size of

the gland,which is not always easily assessable with

palpation due to,for example,physical limitations and

surgical scars. The size of the normal thyroid gland var-

ies according to the morphotype of subjects,reaching

7±8 cm in length with only 0.7±1.0 cm as thickness in

thin subjects,whereas in obese patients the length is

usually less than 5 cm,but the normal anteroposterior

diameter can reach 2 cm. Being volumetric studies of

thyroid lobes easily performable only with 3D ultra-

sound (not yet widely available),thus far thickness is

considered the simplest among the most reliable indexes

of thyroid size: when it is larger than 2 cm,enlargement

can be confidently diagnosed [1,2,3].

The normal thyroid parenchyma has a characteristi-

cally homogeneous ultrasound appearance which is

more echogenic than the adjacent strap muscle and well

distinguishable from the many relevant adjacent struc-

tures,i.e. trachea,esophagus,nerves,large blood vessels.

Eur. Radiol. (2001) 11: 2411±2424

DOI 10.1007/s00330-001-1163-7

ULTRASOUND*

Luigi Solbiati

Valeria Osti

Luca Cova

Massimo Tonolini

Ultrasound of thyroid, parathyroid glands

and neck lymph nodes

Published online: 25 October 2001

 Springer-Verlag 2001

* Categorical Course ECR 2002

L.Solbiati (

)

) ´ V.Osti ´ L.Cova ´

M.Tonolini

Department of Radiology,General

Hospital of Busto Arsizio,Piazzale Solaro,

3,21052 Busto Arsizio (VA),Italy

E-mail: [e-mail]

Phone: [phone]

Fax: [phone]

Abstract In the past 15 years high-

frequency B-mode sonography and

colour±power Doppler have be-

come the most important and most

widely employed imaging modali-

ties for the study of the neck,in par-

ticular for thyroid gland,parathy-

roids and lymph nodes. Sonography

allows not only the detection but of-

ten also the characterization of the

diseases of these organs,distin-

guishing benign from malignant le-

sions with high sensitivity and speci-

ficity,which could be further im-

proved by the employ of ultrasound

contrast agents and harmonic imag-

ing. Although no single sonographic

criterion is specific for benign or

malignant nature of the lesions,the

combination of different signs can

be markedly helpful to speed up the

diagnostic process. Fine-needle as-

piration biopsy (FNAB) remains the

most accurate modality for the de-

finitive assessment of thyroid gland

nodules and of any doubtful case of

nodal disease. In association with

clinical findings and serum levels of

parathormone,FNAB has specifici-

ty close to 100% for the character-

ization of parathyroid adenomas. A

combined approach with sonogra-

phy and FNAB is generally highly

effective.

Keywords Thyroid gland ´

Parathyroid glands ´ Lymph nodes ´

Ultrasonography ´ Power Doppler ´

Colour Doppler

Thyroid pathologies are classifiable into two groups,

nodular and diffuse diseases.

All thyroid diffuse diseases (with the exception of the

extremely rare diffuse primary lymphoma) and approx-

imately 90±92 % of nodular pathologies are benign [4].

Actually,thyroid cancer is rare,accounting for less than

1% of all malignant neoplasms [5]. Sonography is sig-

nificantly more sensitive than clinical palpation in iden-

tifying thyroid nodules [6] and in detecting multinodu-

larity when single nodules are clinically diagnosed.

Studies comparing clinical palpation with thyroid imag-

ing show a prevalence of 13±50% for the detection of

thyroid incidentalomas [7,8]. In recent years,high-res-

olution sonography has confirmed the pathological

statement that multinodularity does not necessarily

mean benign disease or does not exclude malignancy

(Fig. 1) [4,6],being the rare thyroid malignancies often

found in association with one or more benign nodules,

both in the same and in the opposite thyroid lobe. Since

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

As for detection and characterization,each thyroid

nodule has to be studied paying attention to its level of

echogenicity compared with the normal parenchyma,

the presence of calcifications or cystic changes,the pat-

tern of margins,the presence of peripheral echo-poor

ªhaloº and the amount and distribution of blood supply

[3,9,10,11].

Hyperplasia is the most common pathology of thy-

roid gland,accounting for 80±85% of all thyroid nod-

ules,and is more common in women [12]. It may be fa-

milial,due to iodine deficiency,to compensatory hyper-

trophy or secondary to hypoplasia of one lobe or partial

thyroidectomy. When single or multiple hyperplastic

nodules lead to a global enlargement of the gland,the

term goiter (either single or multinodular) is properly

used. Patients with hyperplasia/goiter are frequently

asymptomatic but may occasionally present with com-

pressive symptoms or rapidly enlarging mass,usually

indicating spontaneous haemorrhagic changes within

the nodule(s). Hyperplasia may have a diffuse or nodu-

lar pattern. Diffuse hyperplasia results in the enlarge-

ment of one or both lobes,with lateral or posterior de-

viation of the great vessels and/or the trachea,but never

with infiltration of their walls. Mono- or multinodular

hyperplasia is usually seen as single or multiple discrete

nodules,varying greatly in number and size,separated

2412

Fig.1a, b Multinodularity does not exclude malignancy. a Multi-

ple nodules with different echogenicity (isoechoic,mixed,cystic

with dense fluid) in benign goiter. b Two contiguous hypoechoic

nodules with microcalcifications and irregular margins: multifocal

papillary carcinoma

by normal parenchyma. They are mostly isoechoic

(Fig. 2) and hyperechoic with well-defined margins. The

very unusual hypoechoic nodular hyperplasias (5%) are

due to ªsponge-likeº multilocular lesions filled with

colloid substance. Cystic changes are present in 60±70%

of cases,due to either haemorrhages (Fig. 2) or colloid

substance collections: in this latter circumstance,typical

comet tail artefacts are seen within the nodules (Fig. 2).

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-

2413

2 a

2 c

2 b

2 d

3

Fig.2a±d Four different examples of thyroid nodular hyperplasias

with typical features of benign nature: a isoechoic with thin regular

halo and small internal cystic change, b isoechoic with peripheral

vascularity and wide internal fluid-filled area, c cystic with multiple

comet-tail artefacts due to colloid substance and d isoechoic,

markedly hypovascular within a highly vascularized thyroid pa-

renchyma
Fig.3 Thyroid adenoma with characteristic arrangement of the

blood supply: peripheral vascularity with ªspoke-and-wheelº ap-

pearance of the blood vessels towards the centre of the mass

morphic and seen as large,densely calcified areas with

posterior shadowing [4]. As clearly demonstrated by

pathological studies,hyperplastic±goitrous nodules are

usually less vascularized than normal thyroid parenchy-

ma,with the exception of rapidly growing hyperplastic

lesions in young patients. As a consequence,on colour-

power Doppler these nodules usually appear poorly

vascularized,with prevalent perilesional blood supply

(Fig. 3). Unfortunately,with the increasing sensitivity to

slow blood flows of modern power-colour Doppler

technology,a great amount of hyperplastic/goitrous

nodules currently show also intralesional flow signals.

Therefore,the sign of ªexclusively perilesional blood

flow signalsº on colour Doppler is markedly decreasing

its relevance as character of benign nature.

Non-goitrous nodules include mostly adenomas and

carcinomas.

Adenomas represent only 5±10% of all nodular dis-

eases of the thyroid and are more common in women

[5]. Thyroid adenomas may be either hypoechoic,iso-

echoic (like most follicular adenomas) or hyperechoic.

Characteristically,they usually show a thick and smooth

peripheral echo-poor halo,likely representing fibrous

capsule and peripheral blood supply of the tumour.

Even more typically,from the periphery blood vessels

move to the centre of the lesion,with a relatively regular

ªspoke-and-wheelº arrangement which is clearly visible

with colour Doppler (Fig. 4).

Hyperfunctioning thyroid nodules may pathological-

ly be either hyperplastic nodules or adenomas. In this

latter circumstance,hypervascularity (Fig. 5) and typi-

cal blood supply arrangement allow for a highly reliable

recognition of the hyperfunctioning lesion within the

thyroid parenchyma,with reported sensitivity of 96%

and specificity of 75% [13].

Malignant neoplasms of the thyroid gland are quite

rare (2±3 cases per 100,000 individuals).

Papillary carcinoma is the most common malignan-

cy of the thyroid gland (60±70% of all thyroid malig-

nancies) [14]. It affects women more often than males

and is prevalent in patients under 20 and above

70 years of age. Slow growth and good prognosis are

common features of this neoplasm,the reported 20-

year survival rate being as high as 90% [15]. On ultra-

sound papillary carcinoma appears as a predominantly

hypoechoic nodule,mostly solid,even if in 20±30% of

cases cystic changes with detectable blood supply

within intracystic septa may be seen (ªcystic-papillary

carcinomaº; Fig. 6). Intralesional punctate calcifica-

tions (microcalcifications),are characteristically pre-

sent in 85±90% of these tumours and are highly reli-

able for the sonographic diagnosis of papillary carci-

2414

4 a

5 a

5 b

4 b

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.5a, b Papillary carcinoma

with typical features: a hypo-

echogenicity,microcalcifica-

tions and b hypervascularity

with chaotic arrangement

noma (or,much more rarely,of medullary carcinoma;

Fig. 6). With high-frequency ultrasound,they appear

highly echogenic but typically do not exhibit posterior

shadowing. Pathologically,they represent calcified

psammoma bodies,which are a typical landmark of this

disease. On colour-power Doppler,hypervascularity

with chaotic arrangement of blood vessels,related to

arteriovenous shunts and tortuosity of vessel course,is

commonly seen (90% of cases; Fig. 6) [15,16]. The

major route of spread of papillary carcinoma is through

the lymphatics of the neck and therefore laterocervical

and/or recurrent adenopathies are either often associ-

ated with the primary tumour at initial diagnosis (ap-

proximately 50% of cases) [17,18,19] or may develop

after thyroidectomy. These nodes often reproduce the

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%).

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

or follicular carcinomas has been reported [1].

With sonography,anaplastic carcinomas are diffusely

hypoechoic,with areas of necrosis in 78% of cases,

dense amorphous calcifications in 58% and nodal or

distant metastases in 80% [7,21]. Furthermore,even

more diagnostically useful,sonographic signs of this

cancer are marked irregularities of the boundaries and

the early invasion of thyroid gland capsule,with infil-

tration of adjacent structures (Fig. 9).

Medullary carcinomas account for only 5% of all

thyroid malignancies. In 20 % of the cases they may be

familial,occurring in association with the multiple en-

docrine neoplasia (MEN IIA) syndrome. Slow growth

and spread via the lymphatics to nearby lymph nodes

are characteristic features. Medullary carcinomas are

multicentric and/or bilateral in approximately 90 % of

the familial cases. Prognosis is considered to be gener-

ally worse than that for follicular cancer.

The sonographic appearance of medullary carcinoma

is similar to that of papillary carcinoma: hypoechoge-

nicity,irregular margins,microcalcifications (histologi-

cally representing calcified deposits of amyloid),hyper-

vascularity with irregular arrangement of blood vessels)

2415

6

7

Fig.6 Cystic±papillary carcinoma with microcalcifications and

blood vessels in the solid portion of the mass
Fig.7 Thyroid mass with aspecific sonographic features: iso-

echogenicity,no microcalcifications,perilesional and internal

blood supply. The histological diagnosis is follicular carcinoma

and frequent association with metastatic lymphadenop-

athies are the most distinctive features [12,22].

Thyroid primary lymphoma is rare (4% of all thyroid

malignancies),mostly of the non-Hodgkin's type and

usually affects elderly females. The typical sign is a rap-

idly growing mass which may cause symptoms of ob-

struction such as dyspnea and dysphagia. In 70±80% of

cases,thyroid lymphoma arises from a pre-existing

chronic thyroiditis with subclinical or overt hypothy-

roidism [23]. Prognosis is highly variable and depends

on the stage of the disease. The 5-year survival rate may

range from nearly 90 % in early-stage cases to less than

5% in advanced,disseminated disease.

Sonographically,thyroid lymphoma appears as a hy-

poechoic,lobulated,nearly avascular mass. Large areas

of cystic necrosis may occur,as well as encasement of

large blood vessels of the neck. The adjacent thyroid

parenchyma may be heterogeneous due to associated

chronic thyroiditis [23].

Once a thyroid nodule has been detected with

sonography the fundamental problem is to determine

whether it is benign or malignant. For this purpose,all

the different sonographic signs described above (echo-

genicity,margins,peripheral halo,amount and ar-

rangement of vascularity,microcalcifications,invasion

of adjacent structures) have to be singularly analysed

and combined with clinical data in order to differenti-

ate purely benign nodules from lesions requiring cyto-

logical assessment by FNAB,being suspected of ma-

lignancy.

According to our experience and the literature,

rates of likelihood of benign or malignant nature can

be assigned to all the most important sonographic signs

of thyroid nodules. These data are summarized in Ta-

ble 1.

In recent years several papers in the international

literature have reported data concerning the reliability

of sonography (B-mode and colour/power Doppler) in

the differentiation of benign vs malignant thyroid nod-

ules,employing the sonographic features described

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

sonographic studies using microbubbles could further

improve the diagnostic capabilities of sonography. Thus

far,preliminary experiences with the first generation,

galactose-based contrast agent seem to provide useful

data for the differentiation of benign vs malignant nod-

ules through the analysis of the time-intensity curves

correlating the variation of signal intensities during the

contrast transit time [26].

Even though no sonographic feature is pathogno-

monic for malignancy,the high rates of sensitivity and

specificity reported account for the current major role

of sonography among all imaging modalities in thyroid

nodular lesions. Its use is likely to be complementary,

rather than alternative,to FNAB which is the most ef-

fective method for diagnosing malignancy in a thyroid

nodule. The FNAB is reported to have sensitivity ranges

of 65±98% specificity of 72±100%,false-negative rates

of 1±11% and false-positive rates of 1±8% [27,28].

In our opinion,in patients presenting with one or

more palpable thyroid nodules,the initial imaging mo-

dality to be performed should be chosen on the basis of

laboratory tests: if the blood levels of TSH are either

normal or increased,sonography (including colour/

power Doppler) has to be the first imaging test. If no

sonographic signs suggesting malignancy are detected

and no clinical data of possible malignancy (e.g. rapid

growth,hard consistency,history of neck radiotherapy

treatment) are reported,no further assessment is need-

ed and only a 6- to 12-month sonographic follow-up

study is advisable. If even a low probability of malig-

nancy is sonographically suspected,FNAB is the man-

datory further assessment. On the contrary,if TSH lev-

2416

8

9 a

9 b

Fig.8 Large anaplastic carcinoma with irregular margins,posteri-

or extracapsular growth and infiltration of the laryngeal recurrent

nerve (arrow)
Fig.9a, b Patient with family history of multiple endocrine neo-

plasia II A. a In the left lobe of the thyroid gland,there is a large

hypoechoic nodule with thick halo and scattered microcalcifica-

tions. Pathological diagnosis: medullary carcinoma. b On the right

side,typical parathyroid adenoma (oval,hypoechoic,with regular

margins) is seen caudally to the thyroid lobe

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

between diffusely hyperfunctioning thyroid gland and

ªhotº nodules.

As for the increasingly frequent issue of nonpalpable

nodules incidentally detected by sonography,three dif-

ferent criteria (even though with possible overlapping in

some instances) may be followed in the diagnostic work-

up:

1. Size: according to this parameter,all nodules ex-

ceeding 1.0 cm in maximum diameter should be

punctured,irrespective of physical and sonographic

features,whereas lesions under 1.0 cm should be only

followed on time.

2. Clinical±sonographic features: patients with history

of neck irradiation or familial history of MEN dis-

ease and patients presenting with cervical adenopa-

thies with sonographic appearance consistent with

malignancy and thyroid nodule(s) of any size must

undergo ultrasound-guided FNAB of both thyroid

nodule(s) and adenopathies.

3. Purely sonographic features: nonpalpable nodules

showing sonographic features highly suspected for

malignancy should always undergo ultrasound-guid-

ed FNAB [5].

In conclusion,a combined approach with sonography

and FNA in patients with questionable thyroid nodules

is generally highly effective. In fact,the extremely low

probability to develop thyroid malignancies during a 6-

year follow-up period in patients with benign FNA has

been already reported. Consequently,the possibility of

missing a malignancy in a patient in whom both sonog-

raphy and FNAB do not yield malignant features is ac-

tually very small [29].

Diffuse diseases

Several thyroid diseases are characterized by diffuse

rather than focal involvement: acute suppurative thy-

roiditis; subacute granulomatous or De Quervain's thy-

roiditis,and chronic lymphocytic thyroiditis,called

Hashimoto' s disease in its goitrous form [35]; colloid

diffuse goiter and Graves' disease,the commonest cause

of thyrotoxicosis. Diagnosis of these conditions is usu-

ally made on the basis of clinical and laboratory findings

and,on occasion,by FNAB,with a very limited role of

sonography.

In hyperplasia with hyperfunction (Graves' disease)

the gland contours are lobulated and the size is in-

creased,with usually prompt response to effective

medical treatment: size reduction is a useful indicator of

therapeutic success. The echotexture may be more in-

homogeneous than in diffuse goiter,mainly because of

the presence of numerous large intraparenchymal ves-

sels. Furthermore,especially in young patients,the pa-

renchyma may be diffusely hypoechoic either due to the

extensive lymphocytic infiltration or to the predomi-

nantly cellular content of the parenchyma,almost lack-

ing of colloid substance. Colour flow Doppler and

spectrum analysis confirm the hypervascular pattern

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

Well defined

+++

++

Poorly defined

+

+++

Calcification

Eggshell calcifications

++++

+

Coarse calcifications

+++

+

Microcalcifications

+

++++

Doppler

Peripheral flow pattern

+++

+

Internal flow pattern

++

+++

+ rare probability (< 1%); ++ low probability (< 15%); +++ inter-

mediate probability (16±84%); ++++ high probability (> 85%)

Fig.10 Graves-Basedow disease with peak systolic velocities of

approximately 85 cm/s

that Ralls called ªthyroid infernoº: intrathyroid arteries

present turbulent blood flow with arterovenous shunts

and the highest peak systolic velocities found in thyroid

diseases (50±120 cm/s),due to a flow rate usually ex-

ceeding 70 cm/s (Fig. 10).

There are at present no demonstrations of correla-

tion among degree of thyroid hyperfunction assessed on

the laboratory parameters,extent of hypervasculariza-

tion and flow-velocity values. On the contrary,in

Graves' disease it has been demonstrated that the fea-

tures of hypoechoic thyroid parenchyma and high flow

in the thyroid artery and glandular parenchyma prior to

starting medical therapy are highly specific for the pre-

diction of relapse of hyperthyroidism at the end of the

treatment [30]. In the course of medical treatment of

Graves' disease,a significant decrease in flow velocities

of the inferior and superior thyroid arteries is usually

recorded. It is generally directly proportional to the de-

crease of the free fractions of thyroid hormones.

Subacute granulomatous (or De Quervain's) thy-

roiditis is a self-limiting viral disease,usually preceded

by infection of the upper airways. In the initial stage,

transient hyperthyroidism due to massive follicular

rupture has been reported. Subsequently,moderate and

transient hypothyroidism may occur,related to slowly

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

presentation,related to excessive hormonal release

stimulated by antibodies (hashitoxicosis). Following this

phase,hypothyroidism slowly develops,together with

the progression of histological changes,consisting of

lymphocytic infiltration and fibrosis.

The typical sonographic features are increase in size,

lobulated margins,fibrotic septa (ªpseudolobulatedº

appearance) [32] and particularly ªmicronodulationº

[33],namely the dissemination in the whole thyroid pa-

renchyma of hypoechoic rounded spots,commonly

1±6.5 mm in size (Fig. 11). Histologically,they represent

lobules of thyroid parenchyma with massive infiltration

of lymphocytes and plasma cells,surrounded by a hy-

perechoic ring of fibrous strands. Micronodulation is a

highly sensitive sign of chronic thyroiditis,with a posi-

tive predictive value of 94.7 % [33].

With colour Doppler marked intraparenchymal hy-

pervascularity,chiefly arterial,is mostly detected,espe-

cially inside the hyperechoic septa. This pattern does

not differ significantly from the ªthyroid infernoº de-

scribed in Graves' disease,but in chronic thyroiditis

blood flow velocities mostly remain within normal lim-

its,both before and following medical treatment.

The end stage of chronic thyroiditis is the atrophic

form: the thyroid gland is small,with ill-defined margins

and heterogeneous texture due to progressive increase

of fibrosis. Blood flow signals are completely absent.

A quite peculiar,though not exceptional,finding is

the coexistence of thyroid nodules,benign or malignant,

with chronic lymphocytic thyroiditis. Cytology is often

needed to achieve the final diagnosis [34].

2418

Fig.11a, b Chronic lymphocytic thyroiditis. a Severe disease,with

pseudolobules,fibrous septa,irregular margins and very low level

of echoes. b Occult disease with hypoechoic micronodules and

mild irregularities of margins

Painless (silent) thyroiditis has the typical histologi-

cal and sonographic (hypoechogenicity,micronodula-

tion and fibrosis) pattern of chronic autoimmune thy-

roiditis,but clinical symptoms may be completely ab-

sent in most cases (Fig. 11). Usually the detection is oc-

casional during sonographic studies of the neck per-

formed for different purposes. Slow progression to hy-

pothyroidism is a common finding.

In summary,sonography plays a minor role in the

diagnosis and management of diffuse thyroid diseases,

although some sonographic features are nearly pathog-

nomonic of definite diseases. Sonography can be useful

in diagnosing subclinical forms of diffuse disease,in de-

termining the coexistence of nodular lesions and thy-

roiditis,and in monitoring changes in textural and vas-

cular patterns during medical treatment.

Parathyroid glands
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;

however,when there is biochemical evidence of hyper-

parathyroidism (HPT),high-frequency sonography is

commonly used to detect abnormal parathyroid glands,

being a highly accurate non-invasive procedure for this

purpose.

Primary hyperparathyroidism is now recognized as a

common endocrine disease,especially in patients over

50 years old. The three main aetiologies are: adenoma

2419

1

12

2 a

a

13

14 a

14 b

1

12

2 b

b

Fig.12a, b Parathyroid hyperplasias in secondary hyperparathy-

roidism. a Transverse scan of the thyroid gland: large hypoechoic

parathyroid hyperplasia on the right side and small lesion on the

left side. Both lesions are located posteriorly to the thyroid lobes

and show peripheral capsule. b Longitudinal scan of the thyroid

lobe with two small,rounded,hypoechoic and capsulated par-

athyroid hyperplasias
Fig.13 Primary hyperparathyroidism. Large hypervascular par-

athyroid adenoma with both internal and perilesional blood flow

signals
Fig.14a, b Cystic parathyroid tumours. a Highly echogenic par-

athyroid adenoma with wide cystic changes and perilesional blood

flow signals. b Anechoic parathyroid cyst with perilesional blood

supply

(almost always limited to a single gland); hyperplasia

(which involves all four glands); and carcinoma. Ade-

noma is the most common cause of HPT (80% of cases)

[35]. The preoperative localization of parathyroid tu-

mour(s) is highly recommended,since it allows for a re-

markable shortening of operative time,especially when

surgery is complicated by,for example,anatomical pe-

culiarities and abnormal locations of the glands. In ad-

dition,preoperative localization reduces the risk of

damaging the laryngeal nerve and normal parathyroids

[4,36,37].

Secondary hyperparathyroidism is usually a response

to chronic hypocalcaemia in uraemic patients. Since

surgery is advisable only in advanced cases,ultrasound

examination may help the clinical management of these

patients,monitoring size and structure changes during

medical treatment,but may also help the surgical man-

agement,facilitating the detection of enlarged supernu-

merary parathyroid glands or glands in atypical posi-

tions [38].

Parathyroid adenomas and hyperplasias have usually

oval or oblong shape,with longitudinal diameter rang-

ing from 7 to 15 mm. The smallest adenomas can be

minimally enlarged glands that appear virtually normal

during surgery but are found to be hypercellular on

pathological examination Occasionally,the largest ade-

nomas may have tubular shape and exceed 4±5 cm in

longitudinal size. They are mostly homogeneously solid,

markedly more hypoechoic than the adjacent thyroid

tissue. This characteristic hypoechogenicity is due to the

uniform hypercellularity of the gland,which leaves few

interfaces for reflecting sound. Parathyroid lesions are

separated from thyroid tissue by an echogenic plane,

representing the capsule [35]. Most adenomas and hy-

perplasias are hypervascular on colour Doppler,with

prominent diastolic flow (Fig. 12).

In 15±20% there are variations in the echotexture of

parathyroid tumours.

Occasionally,the level of echogenicity can be similar

to that of thyroid parenchyma,increasing the difficulties

for the sonographic differential diagnosis; approxi-

mately 2% have internal cystic components that are due

to cystic degeneration (Fig. 13). More rarely,purely

cystic adenomas may be found (Fig. 13). Solitary par-

athyroid cyst,more frequent in women,occur below the

level of the inferior thyroid margin in 95 % of cases;

65% of them involve the inferior parathyroid glands.

The cystic fluid has high levels of parahormone. Calci-

fications are rare in adenomas and more common in

carcinomas and hyperplasias due to secondary HPT,

because of the long duration of these diseases.

Preoperative serum calcium levels are usually higher

in patients with larger adenomas. When multiple par-

athyroid tumours (either adenomas or hyperplasias) are

present in the same patient,they have the same sono-

graphic and gross appearance as single parathyroid tu-

mours; however,the glands may be inconsistently and

asymmetrically enlarged,and the diagnosis of multiple

gland disease often is difficult to make sonographically.

The appearance may be misinterpreted as solitary ade-

nomatous disease,or the diagnosis may be missed alto-

gether if the glandular enlargement is minimal.

In most cases,parathyroid carcinomas are indistin-

guishable sonographically from large benign adenomas.

Gross evidence of invasion of adjacent structures,such

as vessels or muscles,is the only reliable preoperative

sonographic criterion for diagnosis of malignancy,but

this is an uncommon finding (Fig. 14) [1,4]. Further-

more,benign lesions are mobile when patient swallows,

whereas malignant lesions may be fixed [35].

Parathyroid glands have an extreme variability of

number and location in normal subjects. Most subjects

have four glands which are located posteriorly to the

upper and lower poles of the thyroid gland; however,in

as many as 25% of normal subjects more than four

glands are present [39,40].

When parathyroid tumours are ectopically located,

the sonographic detection may be more difficult: intra-

thyroidal glands (1% of cases) mimic thyroid nodules,

being hypoechoic with well-defined margins. Retro-

tracheal glands are hardly detectable because of the

acoustic shadowing from the trachea. Finally,the unde-

scended glands,situated along the course of the com-

mon carotid artery or the recurrent laryngeal nerve,are

similar to laterocervical lymph nodes [35].

False-positive sonographic diagnoses may be due to

prominent blood vessels,oesophagus,longus colli mus-

cle,thyroid nodules and enlarged cervical lymph nodes,

whereas false-negative results are caused by minimally

enlarged adenomas,adenomas obscured by enlarged

thyroid goiters,and ectopic adenomas.

The sensitivity of ultrasound for the parathyroid ad-

enoma localization in primary HPT ranges between 70

and 80 % [1,41,42,43]. Specificity may be improved

with ultrasound using FNAB. Sonography also permits

the reliable differentiation of parathyroid adenomas

from other pathological structures such as thyroid nod-

ules or cervical lymph nodes [44,45,46]. In persistent or

recurrent hyperparathyroidism,the reported sensitivity

of ultrasound ranges between 36 and 63 % [43,44]. Ul-

trasound augmented by FNAB and PTH assay can lead

to a specificity approaching 100% [47,48].

In conclusion,pre-operative localization of the par-

athyroid glands is useful for the following purposes:

1. To identify one abnormal parathyroid gland: this al-

lows for unilateral neck exploration,thus reducing

operative time and surgical complications.

2. To localize parathyroid tumours in post-operative

either persistent or recurrent HPT: the complication

rate at re-operation is relatively high and the success

rate decreased [36,46].

2420

3. In case of negative results with ultrasound,to aid in

the differential diagnosis of hypercalcaemia which

can be related to causes other than HPT.

Neck lymph nodes
In the normal adult neck there may be up to 300 lymph

nodes,ranging in size from 3 mm to 3 cm. Lymph nodes

are small,oval or reniform bodies lying along the course

of lymphatic vessels. When a node undergoes antigenic

stimulation,it reacts with an increase in size and vascu-

larity [4]. Many pathologies of the head and neck region

present as palpable lymph nodes,most of which are su-

perficially located. Using high-frequency ultrasound,

multiple nodes in all areas of the neck can be detected

and their morphology and vascularity can be thoroughly

assessed; however,due to the different echotexture and

size,it is more difficult to detect benign innocent than

malignant lymph nodes.

Neck lymph nodes can be classified according to

their anatomical location: submental; submandibular;

parotid; facial; deep cervical; spinal accessory; trans-

verse cervical; retropharyngeal; occipital; and mastoid

[4,49,50]. A further topographic classification,per-

formed by AJCC [51],is based on 7 ªlevelsº,usually

employed in order to plan surgical interventions. Lev-

el I includes submental and submandibolar nodes;

levels II,III and IV include deep cervical chain,the

nodes deep to the sternocleidomastoid muscle and the

upper spinal accessory chain. Level V includes the

transverse cervical chain; level VI the anterior cervical

nodes and level VII nodes in the superior mediasti-

num (Fig. 15).

Once lymph nodes are detected,it is mandatory to

define whether they are benign or malignant. For this

purpose,eight parameters should be evaluated: size;

shape; echogenic hilum; level of echogenicity; necrosis;

extracapsular spread; characteristics of vascularity; and

calcifications.

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

from normal nodes. Most inflammatory diseases,except

for granulomatous infections such as tuberculosis,in-

volve lymph nodes diffusely and homogeneously,gen-

erally preserving their normal oval shape (Fig. 16). On

the contrary,the neoplastic infiltration of lymph nodes

occurs primarily in the cortex; therefore,malignant

nodes tend to have a greater transverse diameter,with a

rounded,asymmetrical morphology of the node

(Fig. 16). The long-to-short-axis ratio (L/S ratio) can

be employed for the distinction between benign

(L/S > 2.0) and malignant nodes (L/S < 2.0) [52,53,54,

55,56].

The centrally located,thick and regular echogenic

hilum is a common feature of normal lymph nodes.

Malignant nodes have thin hilum,because of the pe-

ripheral neoplastic infiltration: often the hilum is ec-

centric (or completely lacking),with associated eccen-

tric cortical widening (Fig. 17) [56].

As for the echotexture of the cortex,lymphomatous

nodes have thickened,uniformly hypoechoic cortex,

whereas metastatic nodes show a more echogenic and

heterogeneous cortex. In patients with known primary

cancer,the presence of necrosis in a lymph node is a

highly probable sign of malignancy: it may appear as a

true cystic area or a hyperechoic zone (coagulative ne-

crosis; Fig. 18). Cystic necrosis is also often identified in

tuberculous nodes,commonly located in the spinal ac-

cessory chain and in the supraclavicular region. They

tend to be clumped together,with associated inflamed

surrounding interstitium [56]. Whenever cystic necrosis

is detected in a node,aspiration biopsies for both cytol-

ogy and microbiology studies should be performed.

2421

Fig.15 Parathyroid carcinoma with non-specific sonographic fea-

tures: mild hypoechogenicity and irregular margins

Fig.16 Schematic representation of cervical lymph nodes grouped

in six levels. Level VII is located in the upper mediastinum

Normal lymph nodes have smooth margins. In ma-

lignant transformation nodes have rounded and well-

defined margins. With advancing malignancy,margins

become less defined and sharp,due to possible extra-

capsular spread.

The patterns of vascularity and their changes are

very important in distinguishing between benign and

malignant nodes. Histopathological studies have shown

that arteries and veins enter the node at the hilum and

spread in bundles which course longitudinally with the

long axis of the node. Capillaries arising from these hilar

and medullary vessels feed the nodal cortex [57,58].

Hilar flow with central vascular pattern is seen in most

(98%) benign nodes. On the contrary,most malignant

nodes (78 %) show aberrant vessels with curved course

entering from the nodal capsule,in addition to hilar

vessels (mixed capsular±hilar vascularity; Fig. 19,20)

[59]. The amount of extrahilar vessels is higher in meta-

static nodes than in lymphomatous nodes,which is likely

due to different angiogenesis. Malignant nodes have

pulsatility index (PI) and resistive index (RI) higher

than benign nodes; cut-off values are 1.3 for PI and 0.72

for RI [59,60,61]. Three-dimensional sonography can

be helpful in detecting more easily abnormal vascula-

ture,especially subcapsular and intranodal tortuous

vessels [62].

No single sonographic criterion is absolutely specific

for benign or malignant nature; however,rounded

shape,absence of hilum,irregular or spiculated outline,

coagulative or cystic necrosis,and chaotic capsular

blood flow pattern are signs highly suspicious for ma-

lignancy,especially when they coexist in the same node.

2422

17 a

18

20 a

20 b

19

17 b

Fig.17a, 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
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

For any doubtful case,the most reliable diagnostic mo-

dality is ultrasound-guided FNAB,which is reported to

have accuracy of 89±90%,sensitivity of 76±78 % and

specificity of 98±100% [4,63].

2423

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