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oval nuclei with regular nuclear contours and
conspicuous or inconspicuous nucleoli;
minimal colloid.
Thyroid Hurthle cell lesions fall into the
cytodiagnostic category of indeterminate
lesions (Thy3), and 13% of Hurthle cell lesions
were malignant in one large series [8, 54, 55].
When a Hurthle cell lesion is detected by FNA,
surgical excision is usually indicated for further
histological study [54].
Suspicious of Malignancy (Thy4)
Many cytopathologists use this category when
the cytological features are suggestive of a specific malignancy, but a definitive diagnosis cannot be rendered due to quantitative reasons (i.e.,
malignant appearing cells, but limited cellularity) or qualitative reasons (i.e., focal or less than
well-developed features of malignancy, or an
atypical lymphoid population) [15, 26, 27]. The
most commonly encountered example of this
diagnostic category is ‘‘suspicious for papillary
carcinoma.’’
40
ENDOCRINE SURGERY
Malignant Lesions (Thy5)
The aspirates in this group are diagnostic of
malignancy with unequivocal features of papillary, medullary or anaplastic carcinoma, or of
lymphoma or metastatic tumor [12, 15, 24–27].
These lesions commonly show distinctive cytological features that permit correct identification in the majority of cases. In many of these
cases, diagnosis should be supported by immunocytochemistry (solid tumors) or flow cytometry (lymphomas).
Papillary Carcinoma
This is the commonest form of thyroid cancer,
accounting for up to 80% of thyroid malignancies [56, 57]. It usually presents between 30 and
40 years of age and is three times more common
in women [56, 57]. Clinically, it is often indolent, although certain variants are aggressive. It
tends to spread locally in the neck, compressing
the trachea and may involve the recurrent laryngeal nerve. It can metastasize to lung and
bone.
FNA is highly accurate for the diagnosis of
papillary carcinomas, particularly for classic or
Fig. 3.9. Papillary carcinoma. (A) A cluster of tumor cells
showing nuclear crowding with nuclear grooves and intranuclear inclusions (Papanicolaou stain, 400). (B) Papillary
tissue fragments are seen in a cell block preparation from the
needle washings (H&E stain, 200). (C) The lining epithelial
cells of the papillary fragments are strongly positive for CK19
(immunocytochemistry, 200).
usual type of papillary carcinoma (Fig. 3.9);
more than 90% are reported as malignant
(Thy5) or suspicious (Thy4) on FNA [8, 9, 11,
24–27].
41
FINE-NEEDLE ASPIRATION BIOPSY
Cytological features of papillary carcinoma
include
cellular aspirates;
syncytial aggregates or sheets of cells. May
have papillary cytoarchitecture or psammoma bodies;
enlarged, oval nuclei with eccentric nucleoli;
fine, pale chromatin;
longitudinal nuclear grooves;
intranuclear inclusions;
dense squamoid cytoplasm;
macrophages and debris (evidence of cystic
degeneration), multinucleated giant cells and
variable numbers of lymphocytes;
positive immunostaining for CK19, HBME-1,
and CD44.
Variants of papillary carcinoma include follicular, diffuse sclerosing, Warthin-like, solid, trabecular, cribriform-morular, oncocytic, tall cell,
and columnar cell type [56, 57]. Cytological diagnosis of these less common variants is often
difficult.
Poorly Differentiated Follicular Carcinoma
Follicular carcinoma is the second commonest
form of thyroid cancer, accounting for about
10% of thyroid malignancies [56, 57]. It is
three times as common in women and tends to
present between 30 and 60 years of age. On FNA
biopsy, malignancy is usually suspected due to
the high cellularity, nuclear hyperchromasia
and chromatin coarseness (Fig. 3.10). Some
tumors may show necrosis and mitotic activity.
A cytological diagnosis of insular carcinoma
may be suggested if multiple samples of a thyroid mass are markedly cellular, with a cytological pattern sometimes reminiscent of a follicular
variant of papillary carcinoma. However, the
follicular cells are arranged predominantly in
rosettes, their nuclei appear more monotonous,
although occasional large cells with pleomorphic nuclei may be seen.
Cytological features of poorly differentiated
follicular carcinoma include [9, 24, 25]
highly cellular smears;
cells dispersed and in syncytial multilayered
clusters;
nuclear hyperchromasia, coarse chromatin,
prominent nucleoli, high nuclear cytoplasmic (N:C) ratio;
Fig. 3.10. FNA of a poorly differentiated follicular carcinoma.
(A) Loosely cohesive, pleomorphic tumor cells showing hyperchromatic nuclei and prominent nucleoli (Papanicolaou stain,
400). (B) Similar cells with an apparent mitotic figure are
seen in the air-dried smear (Hemocolor stain, 400).
may have necrosis and mitotic activity;
absence of colloid.
Medullary Carcinoma
This accounts for approximately 5% of thyroid
cancers [56, 57]. About 25% of patients give a
family history. Female preponderance is less
marked comparedwithotherthyroidmalignancies.
Typically, aspirates from a medullary thyroid
carcinoma are hypercellular and show the following cytological features [9, 24, 25]:
Cellular smears, mainly dispersed cells, some
clustering (Fig. 3.11).
Variable cell pattern, plasmacytoid, small
cell, spindle cell.
Moderate anisokaryosis, may have scattered
very large nuclei, bi- and multinucleated
forms.
ENDOCRINE SURGERY
42
Fig. 3.11. Medullary carcinoma. (A) FNA showing dyshesive
plasmacytoid tumor cells with eccentrically located round
nuclei (Hemocolor stain, 200). (B) Thyroidectomy specimen
reveals a solid tumor composed of nests of polygonal tumor
cells with abundant eosinophilic granular cytoplasm. Amorphous amyloid stroma is also evident (H&E stain, 200).
Indistinct nucleoli.
Granular ‘‘salt-and-pepper’’ chromatin.
Background amyloid (approximately 80% of
cases), minimal or no colloid.
Positive immunostaining for calcitonin,
(CEA), and neuroendocrine markers.
Anaplastic Carcinoma
This represents less than 2% of thyroid cancers
[56, 57]. Women are affected more often than
men. It tends to present in the 50 s and 60 s. Half
have metastases at presentation and prognosis
is poor. Where the diagnosis has not been possible on FNA, core biopsy or open biopsy may
assist the diagnosis [9, 24, 25]. Clinical assessment is important to exclude metastatic carcinoma from elsewhere.
Fig. 3.12. FNA of an anaplastic carcinoma. (A) Loosely cohe-
sive spindle-shaped malignant cells with hyperchromatic nuclei
and ill-defined cytoplasm (Papanicolaou stain, 400). (B)
Biopsy shows sarcomatoid anaplastic tumor cells (H&E stain,
400). (C) Tumor cells are positive for cytokeratin MNF116
(Immunohistochemistry, 400).
Diagnostic cytological features of anaplastic
thyroid carcinoma include
highly malignant and bizarre cells: spindle
cells (Fig. 3.12), giant cells, squamoid cells;
43
FINE-NEEDLE ASPIRATION BIOPSY
high-grade nuclear features: marked pleomorphism, dark clumped chromatin, macronucleoli and atypical mitoses.
necrotic cell fragments, debris, inflammatory
background in some tumors;
positive staining for pancytokeratin excludes
sarcoma, lymphoma, or melanoma. However, TTF-1 and thyroglublin stains are
often negative.
Lymphoma
Between 2 and 5% of thyroid malignancies are
lymphomas [56, 57]. The majority of the thyroid
lymphomas are of MALT type and are associated with Hashimoto’s thyroiditis [56, 58].
This often causes special diagnostic problems,
as a mixed cell population including many
plasma cells, suggestive of a florid reactive process, may be seen in smears of low-grade lymphoma. Diagnostic difficulties by FNA biopsy
may be further enhanced by the occurrence of
residual reactive follicles in low-grade MALT
lymphoma. FNA with flow cytometry may provide a diagnosis but core biopsy or open biopsy
may be needed to allow immunohistochemical
subtyping of the lymphoma, which will have
implications for further treatment [12–16].
High-grade diffuse large B-cell lymphoma
(DLBCL) generally presents with a rapidly
enlarging gland clinically suggesting malignancy. The diagnosis is usually obvious in
FNA smears, which show a monotonous population of large lymphoid cells. Hodgkin lymphoma rarely occurs in the thyroid.
Practical points about thyroid lymphomas:
Approximately 50% present with a single
dominant thyroid nodule.
Phenotypically, 28% MALT, 33% DLBCL +
MALT, 38% DLBCL only, 1% follicle center lym-
phoma. Hodgkin lymphoma, plasmacytoma,
and T-cell lymphomas are extremely rare [58].
It is possible to diagnose this on the basis of
FNA where flow cytometry or molecular ana-
lysis can be applied to identify a clonal
population.
Core biopsy or open biopsy may assist the
diagnosis by allowing immunohistochemis-
try to be performed in the context of archi-
tectural features but molecular analysis may
still be required.
The management of patients with thyroid
lymphoma is best given by an appropriate
multidisciplinary group specializing in lymphoma management.
Thyroidectomy is not indicated.
Secondary Tumors
The thyroid is a relatively common site for
metastasis in disseminated malignancy [56,
57]. A metastatic tumor can simulate a primary
neoplasm. Lung, gastrointestinal tract, breast,
kidney, and skin melanoma are the most frequent sites of origin. Cytodiagnosis of metastatic cancer to the thyroid is relatively straightforward as metastatic cancer usually displays a
cytological pattern and immunoprofile distinctive from those of a primary thyroid carcinoma
[59, 60].
Diagnostic Accuracy
and Errors
Thyroid FNA, as with all medical tests, has its
limitations; however, when properly applied, it
is useful in distinguishing low-risk from highrisk or frankly malignant lesions. In a review of
seven large series totaling 18,183 thyroid FNAs,
Gharib and Goellner found that the technique
had a sensitivity rate varying from 65 to 98%
(mean 83%), and that its specificity rate varied
from 72 to 100% (mean 92%) [13]. The falsenegative rate varied from 1 to 11.5% (mean
5.2%), and the false-positive rate varied from 0
to 7.7% (mean 2.9%) [11]. The overall cytodiagnostic accuracy rate of thyroid FNA approached
95% according to some reported series [8, 9, 11,
24, 25].
Successful FNA has been shown to be highly
dependent on operator training and experience
[61]. Equally important is slide preparation,
which requires experience and skill to provide
cellular material that can accurately be interpreted. Inadequate or improper sampling
accounts for a significant portion of false-negative errors [62, 63]. For example, nodules smaller than 1 cm in size may be too small for
accurate needle placement, and nodules larger
than 4 cm in diameter are too large to allow
proper sampling from all areas, thereby
increasing the likelihood of misdiagnosis.
Interpretive errors also account for some false
diagnoses [63]. As mentioned above, FNA
biopsy of thyroid lymphomas may produce
ENDOCRINE SURGERY
44
lymphocytes that can be interpreted as Hashimoto’s thyroiditis, accounting for a false-negative diagnosis [64].
Large-Needle Aspiration
Biopsy and Core Needle
Biopsy
The large-needle-cutting biopsy (also called core
needle biopsy) [65, 66] and the large-needle
aspiration biopsy (LNAB) [67] techniques
employ the largest needles: 14-G Tru-Cut needle
for the former and 16–20 G needles for the latter.
The operator maintains sterility as a skin nick is
performed to permit the insertion of the relatively large needle. Biopsies are performed with
the patient receiving local anaesthesia and can be
performed with or without ultrasound guidance.
These techniques provide a larger tissue
sample that retains its cellular architecture and
permits the use of a range of immunohistochemical stains and, therefore, may enable a
more precise histological diagnosis [65–67].
Reluctance of clinicians to use core needle
biopsy of the thyroid gland, in part, relates to
the perceived risks associated with core-needle
biopsy of the thyroid gland, in particular the
risk of hemorrhagic complications.
Several studies have compared the accuracy
and complications of core needle biopsy with
that of FNA [65–67]. Some have shown
increased diagnostic accuracy when core needle
biopsy and FNA are combined, but the problem
of distinguishing benign and malignant follicular neoplasms remains. In general, the safety
and ease of use of FNA outweigh the slight
increase in accuracy achieved by core needle
biopsy [65, 67]. A comparison of the advantages
and disadvantages of thyroid FNA and core
biopsy is listed in Table 3.3.
Recommendations for Thyroid
FNA Reporting
The most important part of the pathology
report, of course, is the information about interpretation. The report must be clinically relevant
and readily understood by clinicians. The following issues should be addressed in the cytopathology report:
The beginning of the report should include
information about specimen adequacy.
Additional information in the interpretation
component of the report includes the diagnostic category that classifies the specimen
as unsatisfactory or nondiagnostic (Thy1),
benign/nonneoplastic (Thy2), a cellular
lesion suggestive or consistent with a follicular neoplasm (Thy3), suspicious for malignancy (Thy4) or malignant (Thy5).
A specific cytological diagnosis should be provided, and this would be one thatidentifies and
characterizes the nature of the nodule, such
as papillary thyroid carcinoma, medullary
Table 3.3. A comparison of the advantages and disadvantages of thyroid fine-needle aspiration (FNA) and core biopsy
Fine-needle aspiration (FNA) Core biopsy
Easier to perform More difficult to perform
No need for local anesthesia Local anesthesia, skin incision, and sterile technique required
Any size nodule can be sampled Nodules smaller than 1 cm cannot be sampled
Multiple aspirates from different portion of the nodule
can be obtained
Safer and simpler procedure, fewer or no complications More complications (bleeding, injury to laryngeal nerve)
Virtually no seeding of tumor Seeding of tumor reported
Minimal invasive, greater patient acceptance Less patient acceptance (more pain)
Prompt interpretation is possible Longer processing time before interpretation
Lower cost, no expensive laboratory equipment
needed for preparation and staining of smears
Limited material obtained Multiple sections and special stains can be performed easily
Only limited cores from the nodule can be obtained
Higher cost, histology laboratory equipment, and personnel required
for processing of samples prior to interpretation
45
FINE-NEEDLE ASPIRATION BIOPSY
thyroid carcinoma, Hashimoto’s thyroiditis,
follicular neoplasm, colloid nodule.
Ancillary test results, such as immunocytochemistry, should be provided on the report
and reference made to material for ancillary
tests carried out in a separate department
(flow cytometry, molecular biology, microbiological culture and sensitivity).
A final part of the pathology report can
include a recommendation or comment section. This isoptional,but strongly encouraged
when a definitive diagnosis is not rendered.
The recommendation may suggest surgical
treatment, conservative management with follow-up, repeat FNA or further investigation.
Multidisciplinary Meetings
and Quality Assurance
The FNA results should always be taken in clinical context as part of a multidisciplinary team
approach to ensure that future action is most
appropriate for the patient by integrating information from clinical examination, FNA and
biopsy results, nuclear medicine findings, imaging, serology and any other relevant investigations. Good communication with clinicians
through multidisciplinary meeting (MDM) is
recommended to improve the management of
thyroid patients. Where thyroid cancer is managed at a referral center, pathological material
should be received in time to allow sufficient
time for review at the MDM. The cancer center
should provide an expert review by pathologists
with a specialist interest in thyroid disease.
Clinical audit is important for achieving best
results in delivering an FNA service. Different
aspects of the service may be audited to improve
the quality of service. For cytology, these
include auditing nondiagnostic FNA rates and
correlating the histological or clinical outcome
of all diagnostic categories, in particular the
Thy3 category, which as discussed above, is a
heterogeneous group with variable outcomes.
One of the main advantages of a formal classification system (such as Thy1–Thy5) is that it
facilitates clinical audit and allows correlation
of cytology with outcome. However, such systems should not be used alone for diagnosis,
which should include a full text report as discussed above.
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4
Thyroid Imaging
Carmelo Nucera, J. Anthony Parker and Sareh Parangi
Introduction to Thyroid
Imaging
Imaging represents an important diagnostic tool
for both endocrinologist and endocrine surgeons.
Each imaging modality used to image thyroid
lesions has advantages and limitations and
when used in combination with sound clinical
judgment is useful for certain diseases of the
thyroid. Clinicians need to be aware of constantly
changing technologies incorporatedinto the imaging equipment which can affect not only sensitivity and specificity of these tools but can also
change long-standing observations in imaging of
the thyroid. This chapter discusses imaging of the
thyroid gland, with particular emphasis on ultrasound scan (USS), ultrasound-guided fine-needle
aspiration biopsy (USS-FNAB), single photon
nuclear scanning, positron emission-computed
tomography (PET), and computed tomography
(CT). Each imaging modality will be discussed in
general and then as it pertains to imaging of
specific thyroid conditions.
Ultrasound and Thyroid
Imaging
Basics of Ultrasound
Ultrasonography, now almost ubiquitously
used to evaluate the thyroid and seen
universally as the imaging modality of choice
was only firstused to evaluate palpable abnormalities of the thyroid in the 1970s [1–3]. Luckily
this imaging modality is not excessively expensive, is easy to learn and can be used in multiple
locations (such as the office, radiology suite, or
operating room), due to its portability. USS
allows measurement of the thyroid gland,
shows tissue echogenicity, vascular flow, and
velocity (color-flow Doppler) and is helpful in
the accurate placement of needles for diagnosticpurposes[4].Itisbestifcliniciansdonot
become intimidated by these user-friendly
machines and familiarize themselves with all
aspects of various machines so they eventually
can use a variety of machines available to them.
During ultrasonography high-frequency
sound waves are generated and used to view
internal organs. Typical diagnostic sonographic
scanners operate in the frequency range of
2–18 MHz. The choice of frequency is a tradeoff between spatial resolution of the image and
imaging depth: lower frequencies produce less
resolution but image deeper into the body.
When the emitted sound encounters a border
between two tissues that conduct sound differently, some of the sound waves bounce back to
the transducer, creating an echo. The echoes are
analyzed by a computer in the ultrasound
machine and transformed into moving pictures
of the organ or tissue being examined. Ultrasound is used in a large array of imaging tools
and frequently for medical diagnostics.
J.G.H. Hubbard et al. (eds.), Endocrine Surgery, Springer Specialist Surgery Series,
DOI 10.1007/978-1-84628-881-4_4, Springer-Verlag London Limited 2009
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