DOI:10.2214/AJR.06.0938
AJR 2007; 188:1706-1715
© American Roentgen Ray Society
Parathyroid Imaging: Technique and Role in the Preoperative Evaluation of Primary Hyperparathyroidism
Nathan A. Johnson1,
Mitchell E. Tublin1 and
Jennifer B. Ogilvie2
1 Department of Radiology, University of Pittsburgh Medical Center and School of
Medicine, 200 Lothrop St., 3950 CHP/MT, Pittsburgh, PA 15213.
2 Department of Surgery, University of Pittsburgh Medical Center and School of
Medicine, Pittsburgh, PA 15213.
Received July 19, 2006;
accepted after revision November 8, 2006.
Address correspondence to M. E. Tublin.
CME This article is available for CME credit. See
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for more information.
FOR YOUR INFORMATION
This article is available for CME credit. See
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for more information.
Abstract
OBJECTIVE. This article discusses the commonly used techniques for
imaging the parathyroid glands and their role in the preoperative evaluation
of patients with primary hyperparathyroidism.
CONCLUSION. The importance of sonography and sestamibi scintigraphy
in the preoperative evaluation of patients with primary hyperthyroidism has
increased with the adoption of minimally invasive parathyroidectomy techniques
at most medical centers. When the results of these studies are concordant, the
cure rates of minimally invasive surgery equal those of traditional bilateral
neck exploration.
Keywords: head and neck imaging • hyperparathyroidism • nuclear medicine • sonography • thyroid gland
Introduction
Primary hyperparathyroidism, whether caused by an adenoma or hyperplasia,
can be cured surgically with a high rate of success. When performed by
experienced surgeons, traditional surgical therapy—bilateral four-gland
exploration—is successful in more than 95% of cases
[1]. The development of
unilateral and focused surgical approaches over the past decade, however, has
made it even more imperative for imaging to accurately locate abnormal
parathyroid glands before surgery. With optimized preoperative mapping, the
success rate of these less invasive techniques equals that of the traditional
bilateral approach
[2–7].
The purpose of this article is to review the imaging techniques and
rationale for the preoperative localization studies that are frequently used
before parathyroidectomy. After a brief review of relevant anatomy and the
physiology of primary hyperparathyroidism, we present current surgical
approaches. The commonly used noninvasive imaging techniques—sonography,
scintigraphy, CT, and MRI—will be discussed. Sonography and
99mTc-sestamibi scintigraphy will be emphasized because these have
clearly emerged as dominant, and potentially complementary, techniques in the
preoperative evaluation of primary hyperparathyroidism.
Embryology and Anatomy
Autopsy series show two superior and two inferior parathyroid glands in
most individuals (Fig. 1).
Supernum erary glands are seen approximately 3–5% of the time, and fewer
than four glands are found in up to 3% of patients
[8,
9]. The superior glands are
derived from the fourth branchial pouch along with the lateral lobes of the
thyroid; the inferior glands arise from the third branchial pouch along with
the thymus gland. These embryologic relationships help to explain the
normal—and variable—anatomic locations of the superior and
inferior parathyroid glands.
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Fig. 1 —Diagram shows posterior view of typical locations of paired
superior (white arrows) and inferior (arrowheads)
parathyroid glands and their relationship to thyroid gland and surrounding
structures. Note close relationship parathyroid glands have with recurrent
laryngeal nerves (black arrows), illustrating why nerve injury is a
significant concern of endocrine surgeons, particularly with four-gland
explorations.
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Fig. 2 —Sonogram of 25-year-old woman with possible thyroid
enlargement (thyroid was normal). Note subtle isoechoic parathyroid gland
inferior to lower pole of thyroid (arrows). Normal parathyroid glands
are uncommonly seen on sonography because of their small size.
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The superior glands tend to be more consistent in location with most (>
90%) glands located deep in relation to the mid portion of the superior pole
of the thyroid near the cricothyroid junction. Infrequently, the superior
glands can be seen more inferiorly, deep in relation to the mid pole of the
thyroid lobes (4%), or they may be located at or above the most superior
aspect of the thyroid (3%). Rarely, the superior glands can be found in the
retropharyngeal (1%) or retroesophageal (1%) spaces or in the thyroid gland
itself (0.2%) [8,
9].
The inferior parathyroid glands are more variable in location but most
commonly are located inferior, posterior, or lateral to the lower thyroid pole
(69%). Because of their common origin with the thymus gland, they can also
commonly be found more inferiorly in the neck, in the thymic tongue, or in the
cervical portion of the thymus (26%). Very rarely, the inferior parathyroid
glands can fail to descend with the thymus and may remain cephalad to the
superior glands. Inferior glands can also be found in the anterior mediastinum
with the thymus (2%) or even inferior to the thymus gland in the mediastinum
(0.2%) [8,
9].
The average size of a normal parathyroid is 5 x 3 x 1 mm;
normal glands weigh between 40 and 50 mg. They are thus infrequently
identified at imaging [10]
(Fig. 2). Adenomas, on the
other hand, are considerably larger; they have a mean mass of greater than 10
times the normal parathyroid gland and are thus often identified at
cross-sectional imaging [11].
Hyperplastic glands can be quite variable in size, both within the same
patient and among populations, but they tend to have a total gland volume
comparable to that of adenomas
[12].
Pathophysiology of Primary Hyperparathyroidism
The parathyroid glands are responsible for calcium homeostasis via the
production of parathyroid hormone (PTH). PTH raises the serum calcium level by
promoting the renal tubular absorption of calcium, decreasing tubular
reabsorption of phosphate, and stimulating osteoclasts. In addition, PTH
stimulates vitamin D production, which, in turn, raises serum calcium by
promoting its absorption by the gastrointestinal tract. Primary
hyperparathyroidism is considered to be present when serum calcium is elevated
and PTH is increased or inappropriately normal. The condition is most commonly
diagnosed in the fifth through seventh decades of life and is a common
endocrine disorder affecting approximately one in 500 women and one in 2,000
men. There are numerous, often nonspecific, clinical manifestations of
hypercalcemia. The most common presenting symptoms include fatigue,
hypertension, bone pain, muscle weakness, and psychiatric illness
[13].
Most cases of primary hyperparathyroidism are caused by a single
parathyroid adenoma (89%). Other causes include hyperplasia of all four glands
(6%), double adenomas (4%), and, rarely, parathyroid carcinoma
[2]. In most instances,
parathyroid adenomas are sporadic. There is an increased incidence of
parathyroid hyperplasia in multiple endocrine neoplasia, type I and multiple
endocrine neoplasia, type IIA, although the incidence of these disorders is
not sufficiently high to justify screening in all instances of primary
hyperparathyroidism [14].
Another rare cause of primary hyperparathyroidism is familial hypocalciuric
hypercalcemia, an autosomal dominant condition that produces PTH-dependent
hypercalcemia. It is associated with mild parathyroid hyperplasia, but
subtotal parathyroidectomy is not an effective treatment and is
contraindicated in these cases.
Current Surgical Approach
Preoperative imaging is less critical for the endocrine surgeon when a
traditional bilateral cervical dissection is used for parathyroid exploration.
A transverse cervical incision made approximately 2 cm above the sternal
notch, just below the cricoid cartilage, permits identification of all four
glands and allows access to nearly all ectopic parathyroid sites. In solitary
adenoma cases, all four glands are sampled and the adenomatous gland is
resected. Treatment success using this approach exceeds 95%. Imaging is used
only after failed initial surgery. For multigland disease, the approach
involves either a subtotal 3.5-gland resection with cryopreservation or a
total parathyroidectomy with autotransplantation into the forearm or neck
muscle.
Over the past decade, the development of minimally invasive approaches to
parathyroid surgery has made accurate preoperative localization of parathyroid
disease absolutely critical for effective surgical treatment. Currently
practiced minimally invasive techniques include unilateral open
parathyroidectomy, video-assisted parathyroidectomy, and videoscopic
parathyroidectomy. All of these techniques involve a more focused approach,
limiting the dissection to the abnormal parathyroid gland and thus
substantially decreasing operative time. The unilateral open technique
involves a small unilateral transverse or lateral incision positioned for
access to the parathyroid adenoma. The video-assisted technique is performed
without insufflation, using a 5-mm endoscope and small conventional
instruments through a 1.5-cm midline incision to identify and resect the
abnormal gland or glands. Videoscopic techniques use carbon dioxide
insufflation to create a working space for dissection and use three small
incisions and endoscopic instruments to remove the abnormal gland, usually
from a lateral cervical approach.
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Fig. 3A —44-year-old woman with hyperparathyroidism due to right
inferior parathyroid adenoma. Resected gland weighed 629 mg, nearly 15 times
weight of a normal gland (40–50 mg). Sonogram shows typical hypoechoic
adenoma (arrows) deep in relation to lower pole of thyroid.
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Fig. 3B —44-year-old woman with hyperparathyroidism due to right
inferior parathyroid adenoma. Resected gland weighed 629 mg, nearly 15 times
weight of a normal gland (40–50 mg). Color Doppler sonogram shows
peripheral feeding vessel (arrow) characteristic of parathyroid
adenomas. Also note typical arc or rim vascularity.
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The extent of minimally invasive parathyroidectomy is often guided by rapid
intraoperative PTH testing. A greater than 50% drop in the serum PTH to normal
or near-normal levels 10 minutes after parathyroid resection accurately
predicts removal of all offending parathyroid tissue. Radioguided
parathyroidectomy, which involves preoperative injection of 99mTc
sestamibi, may also aid the endocrine surgeon in gland localization and may
improve success rates, although this approach is controversial and is used in
very few centers.
Accurate preoperative localization of parathyroid adenomas, particularly
when combined with intraoperative PTH assays, enables use of these less
invasive techniques; numerous studies comparing unilateral with bilateral
approaches have shown similar success rates when preoperative imaging is
highly suggestive of single-gland disease
[7,
15–18].
Cases of suspected multiglandular disease and those with equivocal
preoperative localization still require the traditional bilateral cervical
approach because imaging studies have been shown to have low sensitivity for
the detection of hyperplasia and double adenomas. In addition, the surgical
treatment for hyperplasia requires a bilateral approach; moreover, double
adenomas are bilateral in most cases. Thus, the primary benefit of
preoperative imaging studies is the accurate determination of uniglandular
disease to help select patients most appropriate for unilateral and minimally
invasive approaches.
Imaging is also important in the small percentage of cases of failed
initial parathyroidectomy. Failures are most commonly due to undetected
multiglandular disease but may also be due to ectopic glands or incomplete
resection of a parathyroid tumor. Imaging studies can help to locate the
offending tissue in these cases, facilitating a more focused approach and
fewer surgical complications. In addition, these patients may benefit from MRI
or CT of the mediastinum to search for ectopic parathyroid glands.
Parathyroid Imaging
Sonography and 99mTc-sestamibi scintigraphy are the dominant
imaging techniques for preoperative location of parathyroid adenomas. Numerous
studies comparing these techniques suggest similar sensitivities and
specificities for solitary adenoma detection. Localization accuracy is also
improved when both studies are obtained preoperatively
[2,
19–22].
Contrast-enhanced CT and MRI can also effectively locate parathyroid adenomas
but are less commonly used for preoperative location and are more commonly
used in the setting of failed parathyroidectomy for the detection of suspected
ectopic—often mediastinal—glands. Rarely, cross-sectional imaging
will be used if the findings at sonography and 99mTc-sestamibi
scintigraphy are discordant.
Sonography
Technique
The patient should be scanned supine with a pillow beneath the shoulders to
slightly hyperextend the neck. Gray-scale imaging should be performed with a
high-frequency linear transducer; the study should include longitudinal images
extending from the carotid artery to midline and transverse images extending
from the hyoid bone superiorly to the thoracic inlet inferiorly. Scanning at
12–15 MHz is possible with currently available higher level platforms.
Having the patient swallow under real-time observation may help show inferior
glands located deep in relation to the clavicles
[23]. The thyroid is also
imaged and nodules, particularly those with worrisome sonographic features
(e.g., microcalcifications, lobulation), are documented. The size and volume
of both lobes are also recorded.
Gray-scale imaging is supplemented by color and power Doppler imaging to
look for feeding vessels and vascularity of suspected adenomas shown at
initial gray-scale imaging. Graded compression of subcutaneous tissues and
strap muscles may also be helpful in difficult-to-scan patients.
Imaging Findings
Parathyroid adenomas are nearly always homogeneously hypoechoic to the
overlying thyroid gland on gray-scale imaging and are commonly detected using
gray-scale imaging alone when they are larger than 1 cm in diameter
(Fig. 3A). Hypoechogenicity may
be a result of the marked, compact cellularity that is characteristic of
adenomas at sectioning. They are usually oval or bean-shaped, but larger
adenomas can be multilobulated. Color and power Doppler imaging commonly show
a characteristic extrathyroidal feeding vessel (typically a branch off the
inferior thyroidal artery), which enters the parathyroid gland at one of the
poles (Fig. 3B). Internal
vascularity is also commonly seen in a peripheral distribution. The artery
feeding the adenoma tends to branch around the periphery of the gland before
penetrating deeper, resulting in a characteristic arc or rim of vascularity.
In addition, color Doppler sonography of the overlying thyroid gland may show
an area of asymmetric hypervascularity that may help to locate an underlying
adenoma
[24–26].
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Fig. 4A —55-year-old woman with primary hyperparathyroidism due to
large left superior adenoma. Sonogram shows hypoechoic nodule suspected of
being parathyroid medial to common carotid artery (arrow).
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When gray-scale and Doppler imaging fail to show an abnormal parathyroid
gland, graded compression may show a relatively incompressible gland to help
differentiate an adenoma from surrounding soft tissue
[26] (Fig.
4A,
4B). This technique is often
helpful in detection of ectopic glands in the lower neck.
Normal parathyroid glands average 5 x 3 x 1 mm and are
uncommonly seen with sonography; the histology of the normal parathyroid
gland—chief cells, fibrovascular stroma, and adipocytes—may
account for the isoechogenicity of the gland relative to adjacent thyroid.
Hyperplasia is also a more difficult diagnosis to make sonographically because
the single gland size is generally much smaller than an adenoma
[12] (Fig.
5A,
5B,
5C,
5D). However, as with
adenomas, compact cellularity may render hyperplastic glands hypoechoic
relative to the overlying thyroid.
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Fig. 5A —15-year-old girl with hyperparathyroidism due to parathyroid
hyperplasia. Sonograms show four slightly enlarged parathyroid glands
(arrows): right superior (A), right inferior (B), left
superior (C), and left inferior (D). Patient subsequently
underwent four-gland exploration and subtotal parathyroidectomy, leaving
portion of right superior gland. Largest of resected hyperplastic glands
weighed only 322 mg. Relatively small size of typical hyperplastic glands
decreases sensitivity of sonography.
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Fig. 5B —15-year-old girl with hyperparathyroidism due to parathyroid
hyperplasia. Sonograms show four slightly enlarged parathyroid glands
(arrows): right superior (A), right inferior (B), left
superior (C), and left inferior (D). Patient subsequently
underwent four-gland exploration and subtotal parathyroidectomy, leaving
portion of right superior gland. Largest of resected hyperplastic glands
weighed only 322 mg. Relatively small size of typical hyperplastic glands
decreases sensitivity of sonography.
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Fig. 5C —15-year-old girl with hyperparathyroidism due to parathyroid
hyperplasia. Sonograms show four slightly enlarged parathyroid glands
(arrows): right superior (A), right inferior (B), left
superior (C), and left inferior (D). Patient subsequently
underwent four-gland exploration and subtotal parathyroidectomy, leaving
portion of right superior gland. Largest of resected hyperplastic glands
weighed only 322 mg. Relatively small size of typical hyperplastic glands
decreases sensitivity of sonography.
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Fig. 5D —15-year-old girl with hyperparathyroidism due to parathyroid
hyperplasia. Sonograms show four slightly enlarged parathyroid glands
(arrows): right superior (A), right inferior (B), left
superior (C), and left inferior (D). Patient subsequently
underwent four-gland exploration and subtotal parathyroidectomy, leaving
portion of right superior gland. Largest of resected hyperplastic glands
weighed only 322 mg. Relatively small size of typical hyperplastic glands
decreases sensitivity of sonography.
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Cervical lymph nodes can commonly be mistaken for parathyroid glands.
Central compartment lymph nodes may be particularly prominent when the patient
has coexistent lymphocytic thyroiditis (Figs.
6A and
6B). Several features may help
in distinguishing lymph nodes from adenomas, however. An echogenic fatty hilum
usually indicates a benign lymph node. At color Doppler examination, lymph
nodes are supplied by small hilar vessels, whereas a polar, peripheral
distribution of color flow is commonly seen with parathyroid adenomas
[25,
27]
(Fig. 6C).
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Fig. 6C —25-year-old woman with Hashimoto's thyroiditis. Color Doppler
sonogram may aid in differentiating between lymph nodes and adenomas: Lymph
nodes are supplied by a central hilar vessel (arrow), whereas vessels
that supply adenomas typically enter either pole.
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Concomitant thyroid disease also contributes to imaging pitfalls. Enlarged
multinodular thyroid glands can limit the sonographic evaluation of
parathyroid adenomas: Anatomy is distorted and posterior nodules may mimic
parathyroid disease. Posterior thyroid nodules can have a similar sonographic
appearance to intracapsular parathyroid glands, although the typical vascular
pattern of a parathyroid adenoma is uncommonly seen in thyroid nodules
(Fig. 7). The rare
intrathyroid parathyroid gland is difficult, if not impossible, to distinguish
from a thyroid nodule.
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Fig. 7 —67-year-old woman with hyperparathyroidism and left
tracheoesophageal groove adenoma that could easily be mistaken for posterior
thyroid nodule. Peripheral, polar vascularity seen on color Doppler sonogram
helps to identify this as adenoma. Subsequent parathyroidectomy preformed at
time of total thyroidectomy revealed this to be a supernumerary hyperplastic
parathyroid gland.
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Some ectopic glands can be difficult to detect sonographically,
particularly those in the retrotracheal region, because of the poor acoustic
window caused by the tracheal air column. Sonography has poor sensitivity for
detecting ectopic glands in the mediastinum as well.
Sonographically Guided Percutaneous Biopsy and Ethanol Ablation
In cases in which a more definitive preoperative localization is necessary
and sonographic findings are equivocal, sonographically guided fine-needle
aspiration (FNA) of the suspected gland with subsequent PTH assay has been
shown to be a safe and highly specific technique to confirm whether the
suspected lesion is parathyroid tissue
[28–30].
A study by Stephen et al. [28]
of 57 preoperative sonographically guided FNAs in 54 patients found a
specificity of 100% and no false-positive findings. The three false-negative
FNAs occurred when small glands were sampled. Although PTH aspiration is
rarely necessary for routine cases, this procedure can be particularly helpful
in cases in which prior thyroid or parathyroid surgery has distorted neck
anatomy or when preoperative confirmation of unusual-appearing or ectopic
glands is needed. A theoretic complication of the procedure is seeding of
abnormal parathyroid tissue along the biopsy track, resulting in an entity
known as parathyromatosis. This has been described in cases of recurrent
hyperparathyroidism after parathyroidectomy in which the capsule of the
parathyroid gland was disrupted during the procedure. However, a study by
Kendrick et al. [31] followed
81 patients after percutaneous parathyroid FNA for a mean of 5.8 years and
found no cases of parathyromatosis.
Although it is primarily used as a therapy to treat tertiary
hyperparathyroidism (most often in the setting of renal failure),
sonographically guided parathyroid ablation with ethanol is a potential
treatment option for patients with primary hyperparathyroidism. The procedure
involves placement of the needle in the parathyroid gland and slowly injecting
a volume of ethanol equal to approximately 50% of the volume of the gland
until the absence of blood flow to the gland is confirmed on color Doppler
sonography [32]. Because
surgery is more effective at achieving a long-term cure for primary
hyperparathyroidism, this procedure is mostly used in the setting of
prohibitive risk due to medical comorbidities or a high risk of surgical
morbidity in reoperative cases
[32,
33].
Effectiveness of Preoperative Localization and Role in Surgical Planning
Reported sensitivities for the detection of solitary parathyroid adenomas
with preoperative sonography range from 72% to 89% in recent large series
[34–37].
A meta-analysis performed by Ruda et al.
[2] encompassing 54 studies
performed between 1995 and 2003 using sonography for preoperative localization
in primary hyperparathyroidism calculated sonographic sensitivities for the
detection of solitary adenoma, hyperplasia, and double adenoma to be 79% (95%
confidence interval, 77–80%), 35% (95% confidence interval,
30–40%), and 16% (95% confidence interval, 4–28%),
respectively.
Although much of the literature on this topic is retrospective, Siperstein
et al. [37] recently published
one of the largest prospective studies, involving 350 patients with primary
hyperparathyroidism who underwent preoperative sonography. This study was
unique in that initially a focused unilateral parathyroidectomy was attempted
based on preoperative localization studies, and intraoperative PTH assays were
performed irrespective of the success of the initial focused
parathyroidectomy. Thereafter, all patients underwent a four-gland exploration
to determine where there was any additional parathyroid abnormality that was
not suspected on preoperative evaluation. In this manner, the success of a
focused parathyroidectomy based on preoperative imaging studies could be
estimated, but there was pathologic analysis of all glands in each patient.
Given preoperative sonographic findings suggestive of a single adenoma, a
unilateral approach would yield a single abnormal gland at the correct site in
74% of patients. If it was assumed that the operation would be converted to a
bilateral approach if no adenoma was found on the abnormal side, the surgical
success rate was improved to 90%. This is somewhat lower than the cure rate of
95–97% reported in retrospective series of focused techniques. A
selection bias may explain the discrepancy: Prior retrospective series of
focused techniques have included stratified patient cohorts with diagnostic
preoperative mapping, whereas in the study by Siperstein et al., all subjects
were ultimately subjected to traditional surgical exploration.
Another prospective study by Rickes et al.
[34] involving 98 patients
with primary hyperparathyroidism suggests that particular sonographic
findings—namely, a polar feeding vessel—significantly increase
specificity for detecting parathyroid adenomas. Of those suspected adenomas
that showed a feeding vessel using color Doppler sonography, the abnormal
gland was correctly identified 93% of the time. For the 40% of suspected
adenomas without a visualized feeding vessel, localization was correct only
39% of the time. These findings are similar to those in the retrospective
study of Lane et al. [25],
which found that a prominent feeding artery increased accuracy of localization
from 73% to 88%.
Series in which endocrine surgeons performed parathyroid sonography before
surgery have reported similar results. Solorzano et al.
[36] retrospectively studied
226 patients with primary hyperparathyroidism and found preoperative
sonography correctly identified all abnormal glands 77% of the time. The study
of Milas et al. [38] involved
350 patients, and sonography correctly identified the site in 72% of patients.
These studies suggest the importance of a detailed knowledge of cervical
anatomy and of operator experience in the successful use of sonography for
preoperative localization.
Multiple studies confirm the poor sensitivity of sonography for the
detection of double adenomas. In the study of Haciyanli et al.
[39], 21 of 287 consecutive
patients were found to have double adenomas. A retrospective analysis of
preoperative sonography showed a 40% sensitivity for detection of both
adenomas [39]. Similarly, Sugg
et al. [40] found 23 cases of
double adenoma in 233 consecutive patients, and sonography had a 23%
sensitivity. The similarly low sensitivities seen with 99mTc
sestamibi, a relatively operator-independent technique, might suggest double
adenomas are an inherently different disease process than the typically easily
shown solitary adenoma.
Given the significant operator dependence of parathyroid sonography,
comparisons between studies is particularly difficult. In addition,
substantial advancements in sonography technology over the past 10 years
likely will improve the ability of sonography to detect very small structures
with specific vascular patterns, such as adenomas. In our recent experience, a
high-quality sonographic examination is often sufficient for preoperative
mapping of adenomas; nuclear medicine studies, although still routinely
performed before attempted focused resection, often add little, although they
may be helpful when sonography is nondiagnostic (e.g., with ectopic
parathyroid adenomas). A well-performed sonographic examination also aids the
surgeon because the adenoma location is precisely described. Moreover,
preoperative evaluation of thyroid nodules (with sonographically guided FNA)
can often be performed in the same setting. Clearly, an up-to-date assessment
of the ability of state-of-the-art sonography to identify and locate
parathyroid adenomas as a stand-alone technique is needed.
Parathyroid Scintigraphy
Sestamibi with 99mTc is the most commonly used radiotracer for
imaging the parathyroid glands and has been extensively studied in the setting
of primary hyperparathyroidism. Sestamibi is taken up by both the thyroid and
parathyroid glands, but adenomatous and hyperplastic parathyroid tissue shows
more avid uptake of the radiotracer and often retains the radiotracer longer
than adjacent thyroid tissue. Thus, initial planar images obtained shortly
after the administration of radiotracer will show both thyroid and parathyroid
tissue. Asymmetric foci of increased radiotracer uptake on early images can be
seen, representing abnormal parathyroid tissue superimposed on the normal
thyroid. Delayed images, obtained approximately 2 hours after radiotracer
administration, are acquired to look for foci of retained radiotracer
characteristic of hyperfunctioning parathyroid tissue (Fig.
8A,
8B).
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Fig. 8A —52-year-old woman with hyperparathyroidism and right superior
parathyroid adenoma. Early-phase 99mTc-sestamibi SPECT image shows
physiologic uptake in salivary glands and thyroid gland, with focus of more
intense uptake overlying superior pole of right thyroid lobe
(arrow).
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Fig. 8B —52-year-old woman with hyperparathyroidism and right superior
parathyroid adenoma. Two-hour delayed SPECT image shows radiotracer retention
in adenoma (arrow) but clearing of tracer from overlying thyroid.
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SPECT of the neck through a pinhole collimator can help to differentiate
parathyroid activity from the overlying thyroid and has been shown to increase
the sensitivity of scintigraphic parathyroid imaging
[41–43].
Subtraction techniques have also been used to image the parathyroid glands by
administering a second radiotracer taken up only by the thyroid gland. Either
123I or 99mTc pertechnetate can be used in conjunction
with 99mTc sestamibi to produce subtraction images of the
parathyroid glands, although these techniques have not been clearly shown to
be diagnostically superior to nonsubtracted techniques.
The reported sensitivity of 99mTc-sestamibi scintigraphy is
similar to that of sonography. Recent large series using SPECT show
sensitivities for detection of solitary adenomas in the range of 68–95%
[37,
44–46].
The meta-analysis of Ruda et al.
[2] included 96 studies using
99mTc-sestamibi scintigraphy between 1995 and 2003 in the setting
of primary hyperparathyroidism and calculated the sensitivity for detection of
solitary adenomas at 88% (95% confidence interval, 87–89%). Similar to
sonography, sensitivities for detection of hyperplasia and double adenomas
were low, calculated at 44% (95% confidence interval, 41–48%) and 30%
(95% confidence interval, 2–62%), respectively
[2].
Civelek et al. [44]
reported their experience with 338 consecutive patients undergoing
preoperative 99mTc-sestamibi SPECT studies in which the scans were
interpreted with the reviewers blinded to the clinical status of the patient
or results of other imaging tests such as sonography. In this setting,
99mTc-sestamibi SPECT precisely located 90% of solitary adenomas,
73% of double adenomas, and 45% of hyperplastic glands.
In the large prospective study of Siperstein et al.
[37] discussed previously, a
similar analysis using preoperative 99mTc sestamibi alone to direct
a focal approach resulted in proper identification of the site 68% of the
time. As with the results regarding preoperative sonography, this is somewhat
lower than similar retrospective studies.
Jones et al. [47] also
prospectively interpreted preoperative sestamibi scans and found a high
sensitivity for adenomas > 500 mg, with 93% (91/98) accurately located
versus only 51% (18/35) for those < 500 mg. This shows the disadvantage of
the limited resolution of scintigraphic imaging in the setting of smaller
adenomas.
Combined Sonography and Scintigraphy for Preoperative Evaluation of Hyperparathyroidism
A preoperative approach that combines both the anatomic information of
sonography and the physiologic information of scintigraphy has been shown to
predict the presence and location of solitary adenomas more accurately than
either technique alone. Lumachi et al.
[48] retrospectively reviewed
preoperative sonography and 99mTc-sestamibi findings in patients
with proven solitary adenomas and found a combined sensitivity of 95% versus
80% for sonography and 87% for scintigraphy alone. Similarly, Siperstein et
al. [37] predicted 79%
surgical success in their prospective study combining both techniques versus
74% for sonography and 68% for scintigraphy alone. Solorzano et al.
[36], who advocate
preoperative sonography as the only preoperative location test, found that,
used separately, sonography and scintigraphy each correctly predicted
uniglandular disease in 77% of patients, but this increased to 90% when the
techniques were combined. Using concordant results on sonography and
scintigraphy to plan a focal surgical approach has resulted in high cure rates
similar to the traditional bilateral approach. Sonography has the advantage of
being more specific regarding the site of an adenoma in relation to the
thyroid gland. Scintigraphy clearly has an advantage in the detection of
ectopic glands, particularly in the mediastinum.
Both techniques remain similarly insensitive for the detection of
multiglandular disease and double adenomas. Sugg et al.
[40] retrospectively studied
preoperative imaging findings in 23 of 233 patients found to have
multiglandular disease and found that even when combining both techniques,
multiglandular disease was correctly predicted in 30% of patients,
single-gland disease was incorrectly predicted in 30%, abnormal parathyroid
glands were not located in 30%, and discordant results were provided in 10%.
Haciyanli et al. [39]
specifically studied double adenomas and found combined techniques were only
60% sensitive. Even with the addition of intraoperative PTH assays of the
abnormal glands, double adenoma was correctly predicted in 80% of patients,
emphasizing the need for a traditional bilateral approach in patients with
suspected multiglandular disease
[39]. Given that the operation
of choice for both multiglandular disease and double adenomas is a traditional
bilateral approach, some endocrine surgeons have advocated that equivocal,
negative, or discordant results on both preoperative studies warrant a
nonselective approach because a high proportion of these patients will have
multifocal disease. Thus, the role of the radiologist is to provide highly
accurate location of singlegland disease to facilitate focal surgical
approaches. When findings are equivocal, suggestive of multiglandular disease,
or discordant with other imaging tests, this should be clearly stated as well
because these patients will more likely be treated with a traditional
bilateral approach.
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Fig. 9 —40-year-old woman who presented with recurrent hypercalcemia
and hyperparathyroidism after resection of both left-sided glands.
Contrast-enhanced CT scan shows brisk enhancement of 8-mm soft-tissue nodule
(arrow) in mediastinum that correlated anatomically with focus of
radiotracer retention in mediastinum on prior sestamibi SPECT. This was found
to be a hyperplastic right inferior parathyroid gland.
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Fig. 10A —39-year-old woman with left superior adenoma showing typical
MRI signal characteristics. T2-weighted MR image shows increased T2 signal in
adenoma (arrow) relative to thyroid gland and surrounding soft
tissues.
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Fig. 10C —39-year-old woman with left superior adenoma showing typical
MRI signal characteristics. Gadolinium-enhanced T1-weighted image with fat
suppression shows intense enhancement typical of adenomas (arrow).
These imaging characteristics can be indistinguishable from those of lymph
nodes and thus must be interpreted in clinical context and in concert with
other imaging techniques.
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CT
Axial contrast-enhanced thin-collimation CT images through the neck show
intense enhancement in the typical locations for parathyroid tissue in the
setting of adenoma. Scanning from the skull base through the mediastinum has
the additional advantage of detecting most ectopic glands
(Fig. 9). In cases of failed
initial parathyroidectomy, artifacts from surgical clips placed in the neck
often limit the diagnostic quality of CT. Reported sensitivities of CT range
from 46% to 87% [49]. Combined
studies of sonography and CT suggest that supplemental CT will detect few
additional adenomas over sonography alone. Thus, CT is usually reserved for
cases of failed parathyroidectomy or in cases of altered anatomy, in which CT
may aid in operative planning
[50–52].
Recent studies have combined 99mTc-sestamibi SPECT with
coregistered CT in an attempt to improve sensitivity by combining anatomic and
functional information, but results from these initial studies are conflicting
in their conclusions about the added usefulness of CT. More study is required
before the appropriate usefulness of this combined technique is established
[53–55].
MRI
Although less commonly used for preoperative localization than sonography
and scintigraphy, MRI provides similar sensitivity to other techniques in the
detection of abnormal parathyroid tissue
[56,
57]. More commonly, MRI is
used in patients with persistent or recurrent hyperparathyroidism, in whom it
has been shown to be effective in locating remaining abnormal parathyroid
tissue [58].
Images of the neck are generally obtained with an anterior neck surface
coil from the hyoid bone to the sternal notch. Axial T1- and T2-weighted fast
spin-echo sequences are commonly acquired. In instances in which no neck
lesion is identified or an ectopic parathyroid gland is suspected, ECG-gated
axial images of the mediastinum can be effective.
The T1 and T2 characteristics of abnormal parathyroid tissue are variable.
The most common tissue characteristics are intermediate- to low-intensity T1
signal and high-intensity T2 signal (Fig.
10A,
10B,
10C). Less commonly, fibrosis
or old hemorrhage can cause low signal intensity on T1- and T2-weighted
images. Subacute hemorrhage into adenomas can cause high signal intensity on
both T1- and T2-weighted images
[59].
The acquisition of gadolinium-enhanced T1-weighted images with fat
suppression has not been shown to significantly increase detection of adenomas
when they exhibit T2 hyperintensity. However, false-negative studies are most
commonly associated with adenomas that are isointense on T1 and T2 sequences;
the addition of contrast-enhanced images can increase sensitivity for these
cases [57].
Abnormal parathyroid tissue cannot be diagnosed on MRI by signal
characteristics alone because cervical lymph nodes have similar signal
characteristics. Therefore, accurate MRI diagnosis depends on knowledge of the
typical morphology and location of the parathyroid glands and common sites of
ectopic glands.
Conclusion
Over the past decade, the surgical treatment of primary hyperparathyroidism
has changed from predominantly a bilateral approach with four-gland
exploration in all cases to unilateral and focused approaches guided by
preoperative imaging showing single adenomas. Sonography and
99mTc-sestamibi scintigraphy have assumed dominant roles in
preoperative location of solitary adenomas, and focused approaches based on
concordant findings from both techniques have cure rates equal to that of the
traditional approach. Sonography is particularly diagnostic when a typical
polar feeding vessel and peripheral vascularity are shown. Preoperative
identification of multiglandular disease and double adenomas remains poor;
thus, patients with negative, discordant, or equivocal results will commonly
undergo bilateral procedures because of the high incidence of multifocal
disease in patients without definitive preoperative imaging findings. MRI and
CT are generally reserved for cases of failed initial surgery or recurrent
hyperparathyroidism because the prevalence of supernumerary and ectopic glands
is much higher in this select population.
Acknowledgments
We thank Eric Jablonowski for his illustration of normal parathyroid
anatomy.
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Abstract
Introduction
