Ultrasound of Thyroid Parathyroid Gland by pcherukumalla

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									Eur. Radiol. (2001) 11: 2411±2424
DOI 10.1007/s00330-001-1163-7                   U LT R A S O U N D *




Luigi Solbiati                                Ultrasound of thyroid, parathyroid glands
Valeria Osti
Luca Cova                                     and neck lymph nodes
Massimo Tonolini




Published online: 25 October 2001
                                              Abstract In the past 15 years high-       be markedly helpful to speed up the
 Springer-Verlag 2001                        frequency B-mode sonography and           diagnostic process. Fine-needle as-
                                              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 ´
M. Tonolini
                                              ficity, which could be further im-        effective.
                                              proved by the employ of ultrasound
Department of Radiology, General              contrast agents and harmonic imag-        Keywords Thyroid gland ´
Hospital of Busto Arsizio, Piazzale Solaro,
3, 21052 Busto Arsizio (VA), Italy
                                              ing. Although no single sonographic       Parathyroid glands ´ Lymph nodes ´
E-mail: lusolbia@tin.it                       criterion is specific for benign or       Ultrasonography ´ Power Doppler ´
Phone: +39-03 31-69 94 78                     malignant nature of the lesions, the      Colour Doppler
Fax: +39-03 31-32 62 52                       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
papillary carcinoma
                                                                     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].
    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. 2 a±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
comet-tail artefacts due to colloid substance and d isoechoic,            due to ªsponge-likeº multilocular lesions filled with
markedly hypovascular within a highly vascularized thyroid pa-            colloid substance. Cystic changes are present in 60±70 %
renchyma                                                                  of cases, due to either haemorrhages (Fig. 2) or colloid
Fig. 3 Thyroid adenoma with characteristic arrangement of the             substance collections: in this latter circumstance, typical
blood supply: peripheral vascularity with ªspoke-and-wheelº ap-           comet tail artefacts are seen within the nodules (Fig. 2).
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




 8                                             9a                                           9b

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-
tions. Pathological diagnosis: medullary carcinoma. b On the right
                                                                         of sonography (B-mode and colour/power Doppler) in
side, typical parathyroid adenoma (oval, hypoechoic, with regular        the differentiation of benign vs malignant thyroid nod-
margins) is seen caudally to the thyroid lobe                            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
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
  Well defined                       +++               ++             Fig. 10 Graves-Basedow disease with peak systolic velocities of
  Poorly defined                     +                 +++            approximately 85 cm/s
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




 13




                                            14 a


                                                                                            14 b

Fig. 12 a, 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
and show peripheral capsule. b Longitudinal scan of the thyroid        nomonic of definite diseases. Sonography can be useful
lobe with two small, rounded, hypoechoic and capsulated par-           in diagnosing subclinical forms of diffuse disease, in de-
athyroid hyperplasias                                                  termining the coexistence of nodular lesions and thy-
Fig. 13 Primary hyperparathyroidism. Large hypervascular par-          roiditis, and in monitoring changes in textural and vas-
athyroid adenoma with both internal and perilesional blood flow        cular patterns during medical treatment.
signals
Fig. 14 a, 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
                                                                       Parathyroid glands
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
Fig. 20 a Rounded hypoechoic      17 a                                       17 b
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].


References
 1. Solbiati L, Osti V, Cova L, Martinoli C,    14. Yousem DM, Scheff AM (1996) Thy-            25. Okamoto T, Yamashita T, Harasawa A
    Derchi L (2001) The neck. In: Meire H,          roid and parathyroid. In: Som PM, Cur-          et al. (1994) Test performances of three
    Cosgrove D (eds) Abdominal and gen-             tin HD (eds) Head and neck imaging.             diagnostic procedures in evaluating
    eral ultrasound, vol 2. Churchill Living-       Mosby, St. Louis, pp 952±975                    thyroid nodules: physical examination,
    stone, Edinburgh, pp 699±737                15. Solbiati L, Livraghi T, Ballarati E,            ultrasonography and fine needle aspi-
 2. Carlier-Conrads L (1984) L'echoto-              Ierace T, Crespi L (1995) Thyroid               ration cytology. Endocrinol J 41:
    mographie thyroidienne. In: Moreau JF,          gland. In: Solbiati L, Rizzatto G (eds)         243±247
    Carlier-Conrads L (eds) Imagerie diag-          Ultrasound of superficial structures.       26. Spiezia S, Farina R, Cerbone G et al.
    nostique des glandes thyroide et para-          Churchill Livingstone, Edinburgh, pp            (2001) Analysis of color Doppler signal
    thyroides. Vigot, Paris, pp 89±105              49±85                                           intensity variation after Levovist injec-
 3. Solbiati L, Charboneau JW, James EM,        16. Ahuja AT, Chow L, Chick W et al.                tion, a new approach to the diagnosis of
    Hay ID (1998) The thyroid gland. In:            (1995) Metastatic cervical nodes in             thyroid nodules. J Ultrasound Med 20:
    Rumack CM, Wilson SR, Charboneau J              papillary carcinoma of the thyroid: ul-         223±231
    W (eds) Diagnostic ultrasound. Mosby,           trasound and histological correlation.      27. Gharib H, Goellner JR (1993) Fine
    St. Louis, pp 703±729                           Clin Radiol 50: 229±231                         needle aspiration biopsy of the thyroid:
 4. Ahuja AT, Evans RM (2000) Practical         17. McConahey WM, Hay ID, Woolner LB                an appraisal. Ann Intern Med 118:
    head and neck ultrasound. GMM Pub-              (1986) Papillary thyroid cancer treated         282±289
    lishers, London, pp 37±83                       at the Mayo Clinic, 1946 through 1970:      28. Altavilla G, Pascale M, Nenci I (1990)
 5. Tan G, Gharib H (1997) Thyroid inci-            initial manifestations, pathologic find-        Fine needle aspiration cytology of thy-
    dentalomas: management approaches               ings, therapy and outcome. Mayo Clin            roid gland diseases. Acta Cytol 34:
    to non-palpable nodules discovered in-          Proc 61: 978±996                                251±256
    cidentally on thyroid imaging. Ann In-      18. Black BM, Kirk TA Jr, Woolner IB            29. Watters DAK, Ahuja AT, Evans RM
    tern Med 126: 226±231                           (1960) Multicentricity of papillary ade-        et al. (1992) Role of ultrasound in the
 6. Tan G, Gharib H, Reading C (1995)               nocarcinoma of the thyroid: influence           management of thyroid nodules. Am J
    Solitary thyroid nodule, comparison             on treatment. J Clin Endocrinol Metab           Surg 164: 654±657
    between palpation and ultrasonogra-             20: 130±135                                 30. Castagnone D, Rivolta R, Rescalli S
    phy. Arch Intern Med 155: 2418±2423         19. Lang W, Choritz H, Hundeshagen H                et al. (1996) Color Doppler sonography
 7. Grebe SKG, Hay ID (1994) Follicular             (1986) Risk factors in follicular thyroid       in Graves' disease: value in assessing
    cell derived thyroid carcinoma. In: Ar-         carcinomas. A retrospective follow up           activity of disease and predicting out-
    nold A (ed) Cancer treatment and re-            study covering a 14 years period with           come. Am J Roentgenol 166: 203±207
    search. Endocrine neoplasms. Kluwer,            emphasis on morphological findings.         31. Birchall IW, Chow CC, Metreweli C
    Boston, pp 91±140                               Am J Surg Pathol 10: 246±255                    (1990) Ultrasound appearances of de
 8. Kerr L (1994) High resolution thyroid       20. Compagno J (1985) Diseases of the               Quervain's thyroiditis. Clin Radiol 41:
    ultrasound: the value of colour Doppler.        thyroid. In: Barnes L (ed) Surgical pa-         57±59
    Ultrasound Q 12: 21±43                          thology of the head and neck. Dekker,       32. Langer J, Khan A, Nisenbaum H (2001)
 9. Carroll BA (1982) Asymptomatic thy-             Paris, pp 1435±1486                             Sonographic appearance of focal thy-
    roid nodules: incidental sonographic        21. Takashima S, Morimoto S, Ikezoe J               roiditis. Am J Roentgenol 176: 751±754
    detection. Am J Roentgenol 133:                 et al. (1990) CT evaluation of anaplastic   33. Yeh HC, Futterweit W, Gilbert P (1996)
    499±501                                         thyroid carcinoma. Am J Roentgenol              Micronodulation: ultrasonographic sign
10. Espinasse P, Espinasse D (1979) Radio-          154: 1079±1085                                  of Hashimoto's thyroiditis. J Ultra-
    nuclide imaging and echography of thy-      22. Gorman B, Charboneau JW, James EM               sound Med 15: 813±819
    roid nodules. Clin Nucl Med 4: 269±274          et al. (1987) Medullary thyroid carcino-    34. Takashima S, Matsuzuka F, Nagareda T,
11. Solbiati L, Volterrani L, Rizzatto G            ma: a role of high resolution US. Radi-         Tomiyama N, Kozuka T (1992) Thyroid
    et al. (1985) The thyroid gland with low        ology 162: 147±150                              nodules associated with Hashimoto's
    uptake lesions: evaluation by ultra-        23. Kasagi K, Hatabu H, Tokuda Y et al.             thyroiditis: assessment with US. Radi-
    sound. Radiology 155: 187±191                   (1991) Lymphoproliferative disorders            ology 185: 125±130
12. Livolsi VA (1997) Pathology of thyroid          of the thyroid gland: radiological ap-      35. Moreau JF (1987) Parathyroid glands.
    disease. In: Falj SA (ed) Thyroid dis-          pearances. Br J Radiol 64: 569±574              In: Bruneton JN (ed) Ultrasonography
    ease: endocrinology, surgery, nuclear       24. Leenhardt L, Tramalloni J, Aurengo H            of the neck. Springer, Berlin Heidelberg
    medicine and radiotherapy. Lippincott-          et al. (1994) Echographie des nodules           New York, pp 101±129
    Raven, Baltimore, pp 65±104                     thyroidiens: l'echographiste face aux       36. Levin KE, Clark AH, Duh QY et al.
13. Bruneton JN, Normand F (1987) Thy-              exigences du clinicien. Presse Med 23:          (1992) Reoperative thyroid surgery.
    roid gland. In: Bruneton JN (ed) Ultra-         1389±1392                                       Surgery 111: 604±609
    sonography of the neck. Springer, Ber-                                                      37. Russell CF, Laird JD, Ferguson WR
    lin Heidelberg New York, pp 22±50                                                               (1990) Scan-directed unilateral cervical
                                                                                                    exploration for parathyroid adenoma: a
                                                                                                    legitimate approach. World J Surg 14:
                                                                                                    406±409
2424



38. Takebayashi S, Matsui K, Onohara Y          47. Kairaluoma MV, Kellosalo J, Makarai-        56. Ahuja AT, Ying M, Evans RM, King W,
    et al. (1987) Sonography for early diag-        nen H et al. (1994) Parathyroid re-ex-          Metreweli C (1995) The application of
    nosis of enlarged parathyroid glands in         ploration in patients with primary hy-          ultrasound criteria for malignancy in
    patients with secondary hyperparathy-           perparathyroidism. Ann Chir Gynaecol            differentiating tuberculous cervical ad-
    roidism. Am J Roentgenol 148: 911±914           83: 202±206                                     enitis from metastatic nasopharyngeal
39. Livolsi VA (1985) Pathology of the          48. Miller DL, Doppman JL, Shawker TH               carcinoma. Clin Radiol 50: 391±395
    parathyroid glands. In: Barnes L (ed)           et al. (1987) Localisation of parathyroid   57. Semeraro D, Davies JD (1986) The ar-
    Surgical pathology of the head and              adenomas in patients who have under-            terial blood supply of human inguinal
    neck. Dekker, Paris, pp 1487±1563               gone surgery. Noninvasive imaging               lymph nodes. J Anat 144: 221±233
40. Livolsi VA (1994) Parathyroid glands.           methods. Radiology 162: 133±137             58. Gadre A, Briner W, O'Learly M (1994)
    In: Sternberg SS (ed) The thyroid and       49. Bruneton JN, Balu-Maestro C, Marcy              A scanning electron microscope study
    parathyroid: diagnostic surgical pathol-        PY, Melia P, Morou MY (1994) Very               of the human cervical lymph node. Acta
    ogy. Raven, Baltimore, pp 523±560               high frequency (13 MHz) ultrasound              Otolaryngol 114: 87±90
41. Attie JN, Khan A, Rumancik WM et al.            examination of the normal neck: detec-      59. Shirakawa T, Miyamoto Y, Yamagishi J
    (1988) Preoperative localisation of par-        tion of normal lymph nodes and thyroid          (2001) Color/power Doppler sono-
    athyroid adenomas. Am J Surg 156:               nodules. J Ultrasound Med 13: 87±90             graphic differential diagnosis of super-
    323±326                                     50. Rouviere H (1938) Anatomy of the hu-            ficial lymphadenopathy. J Ultrasound
42. Kohri K, Ishikawa Y, Kodama M et al.            man lymphatic system. Edward Broth-             Med 20: 525±532
    (1992) Comparison of imaging methods            ers, Ann Arbor                              60. Chang DB, Yuan A, Yu CJ, Luh KT,
    for localisation of parathyroids tu-        51. Som PM (1992) Detection of metastasis           Kuo HS, Yang PC (1994) Differentia-
    mours. Am J Surg 164: 140±145                   in cervical lymph nodes: CT and MR              tion of benign and malignant cervical
43. Rodriquez JM, Tezelman S, Siperstein            criteria and differential diagnosis. Am J       lymph nodes with colour Doppler
    AE et al. (1994) Localisation proce-            Roentgenol 158: 969±981                         sonography. Am J Roentgenol 162:
    dures in patients with persistent or re-    52. Sakai F, Kiyono K, Sone S et al. (1988)         965±968
    current hyperparathyroidism. Arch               Ultrasonic evaluation of cervical meta-     61. Lencioni R, Moretti M, Armillotta N,
    Surg 129: 870±875                               static lymphadenopathy. J Ultrasound            Bassi AM, Giulio M di, Bartolozzi C
44. Weinberger MS, Robbins KT (1994)                Med 7: 305±310                                  (1996) Differentiation of benign and
    Diagnostic localisation studies for pri-    53. Shozushima M, Suzuki M, Nakasima Y              malignant superficial lymphadenopa-
    mary hyperparathyroidism: a suggested           et al. (1990) Ultrasound diagnosis of           thy: value of high resolution power
    algorithm. Arch Otolarynol Head Neck            lymph node metastasis in head and neck          Doppler US. Radiology 201(P):225
    Surg 120: 1187±1189                             cancer. Dentomaxillofac Radiol 19:          62. Metreweli C, Ahuja AT (1988) Work in
45. Fugazzola C, Bergamo Andreis I, Sol-            165±170                                         progress: 3D colour power angio, does
    biati L (1995) Parathyroid glands. In:      54. Solbiati L, Rizzatto G, Bellotti E et al.       it have a potentially useful role in lym-
    Solbiati L, Rizzatto G (eds) Ultrasound         (1988) High resolution sonography of            phadenopathy? Eur J Ultrasound
    of superficial structures. Churchill Liv-       cervical lymph nodes in head and neck           8:S16±S17
    ingstone, Edinburgh, pp 87±114                  cancers: criteria for differentiation of    63. Van den Brekel MWM, Castelijns JA,
46. Grant CS, van Heerden JA, Charbo-               reactive versus malignant nodes. Radi-          Stel HV, Golding RP, Meyer CNL,
    neau JW et al. (1986) Clinical manage-          ology 169(P):113                                Snow GB (1993) Modern imaging tech-
    ment of persistent and/or recurrent pri-    55. Vassallo P, Wernecke K, Roos N, Peters          niques and ultrasound guided aspira-
    mary hyperparathyroidism. World J               PE (1992) Differentiation of benign             tion cytology for the assessment of neck
    Surg 10: 555±565                                from malignant superficial lymphaden-           node metastases: a prospective compar-
                                                    opathy: the role of high resolution US.         ative study. Eur Arch Otolaryngol 250:
                                                    Radiology 183: 215±220                          11±17

								
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