Morphological Features of Enlarged Parathyroid Glands in B-Mode-Ultrasound

Abstract

Successful preoperative localisation of parathyroid glands is essential for minimal-invasive surgery of hyperparathyroidism. The knowledge of the sonomorphology of the parathyroid glands, therefore, is an important prerequisite. This article shows that the sonomorphology of normal and pathologically transformed parathyroid glands is subject to a wide variety. The often simplified standard description of parathyroid glands as hypoechogenic and oval may lead to false negative cervical ultrasound examinations.

Full text

Introduction
Since Felix Mandl performed the first successful operation in 1925,
the removal of parathyroid glands has remained challenging [1, 2].
For many decades, the intraoperative identification of all parathyr-
oid glands was mandatory even in cases of a single adenoma. This
principle was developed in order to avoid persistent hyperpa-
rathyroidism due to double adenoma or primary hyperplasia. In
addition, this principle was also formulated because physicians
were unable to localise normal and enlarged parathyroid glands
preoperatively. Doppman (1986) claimed that the only localisation
procedure necessary is to look for an experienced parathyroid sur-
geon [3].
In recent years, ultrasound imaging technology has improved sig-
nificantly and has become the first-line imaging modality for cer-
vical soft tissue lesions [4].
As a result of this development of imaging technology, the princi-
ples of parathyroid surgery have changed significantly since Dopp-
Morphological Features of Enlarged Parathyroid Glands
in B-Mode-Ultrasound
S. Rewerk
1
E. Roessner
1
S. Freudenberg
2
F. Willeke
1
Morphologisches Erscheinungsbild vergrßerter Nebenschilddrsen in der
B-Bild-Sonographie
affiliation
1
Chirurgische Universittsklinik Mannheim, Klinikum Mannheim gGmbH, Mannheim
2
Allgemein-, Gefß- und Visceralchirurgie Marienkrankenhaus Siegen, Akademisches Lehrkrankenhaus der
Universitt Marburg, Kampenstr. 51, Siegen
correspondence
OA Dr. med. Stephan Rewerk · Chirurgische Universittsklinik Mannheim, Klinikum Mannheim gGmbH ·
Theodor-Kutzer-Ufer 1–3 · 68135 Mannheim · Tel.: ++ 49/621/3833578 · Fax: ++ 49/621/383733578 ·
E-mail: stephan.rewerk@chir.ma.uni-heidelberg.de
received: 18.3.2005 · accepted: 12.11.2005
bibliography
Ultraschall in Med 2006; 27: 256 –261  Georg Thieme Verlag KG Stuttgart · New York
DOI 10.1055/s-2006-926540 · Published online March 20, 2006
ISSN 0172-4614
Zusammenfassung
Erfolgreiche properative Lokalisationsdiagnostik ist eine wesent-
liche Voraussetzung der minimalinvasiven Nebenschilddrsen-
chirurgie, welche zunehmende Akzeptanz findet. Hierbei spielt
die Kenntnis der sonomorphologischen Erscheinungsformen der
Nebenschilddrsen eine wesentliche Rolle. In der Literatur wird
die Sonomorphologie vergrßerter Nebenschilddrsen hufig ver-
einfacht dargestellt (echoarm und ovalr). Die Vorstellung eigenen
Bildmaterials soll die erhebliche Sonovariabilitt vergrßerter Ne-
benschilddrsen aufzeigen und damit einen Beitrag zum chirurgi-
schen Erfolg leisten.
Schlsselwrter
Zervikaler Ultraschall · Nebenschilddrsen · Sonomorphologie
Abstract
Successful preoperative localisation of parathyroid glands is es-
sential for minimal-invasive surgery of hyperparathyroidism. The
knowledge of the sonomorphology of the parathyroid glands,
therefore, is an important prerequisite. This article shows that the
sonomorphology of normal and pathologically transformed para-
thyroid glands is subject to a wide variety. The often simplified
standard description of parathyroid glands as hypoechogenic and
oval may lead to false negative cervical ultrasound examinations.
Key words
Cervical ultrasound · parathyroid glands · sonomorphology
Pictorial Essay
256

man’s claim 20 years ago [3]. Modern surgery focuses on the com-
bination of successful preoperative localisation and minimal inva-
sive surgical procedures, facilitating a fast recovery [5]. The most
widely used localisation procedure is therefore cervical ultrasound,
often in combination with Sesta-MIBI-Scintigraphy. Even if it is
planned to remove the glands via an open approach, ultrasound
will be useful to avoid persisting or recurrent hyperparathyroidism
[6]. The success rate of ultrasound of the parathyroid glands seems
to be especially dependent on the individual examiner. Frequently,
morphology and presentation of parathyroid glands in cervical ul-
trasound are quite uniformly described as hypoechoic and oval. In-
dependent of any statistical analysis, this article wants to demon-
strate the potentially wide variety of ultrasound appearance of the
parathyroid glands. These variations should be kept in mind when
performing localisation procedures for the guidance of minimal in-
vasive surgery for hyperparathyroidism.
Material and Methods
From 1995 to 2004, all patients undergoing any surgical procedure
for hyperparathyroidism were examined sonographically by dif-
ferent physicians. For this retrospective study, only pictures of ul-
trasound examinations performed by one examiner (S.R.) were in-
cluded. In equivocal cases, the author was asked by colleagues to
perform the investigation. Therefore, a statistical analysis of these
cases did not appear reasonable because they would not consti-
tute a representative sample of the various sonomorphological
features of glands which actually exist in the population. Primary
and secondary hyperparathyroidism were evaluated as well as
MEN patients for ultrasound morphology of parathyroid glands.
Examinations were performed with three ultrasound machines
(GE Logiq 500, Toshiba Powervision 6000, Siemens Sonoline 450).
Linear and curved probes were used with 5–10-MHz. The surgical
correlate of differing ultrasound pictures was confirmed intra-
operatively by the consulting surgeon (e. g. lobated outline, cen-
tral cystic structure, double adenoma).
Embryology and Anatomy
Typically, there are four parathyroid glands, but in 13–20% of
cases, supernumerary or dispersed cell nidi can be found [7–10].
In 5% of cases of primary hyperthyroidism, a fifth parathyroid
gland can be found [11]. Less than four glands are very rare and
are described in less than 3% [9]. The glands’ normal size ranges
from 3–6 mm in an oval shape. Originating from the fourth phar-
yngeal arch, the upper parathyroid glands descend to a dorsocra-
nial position at the crossing of the inferior thyroid artery and the
recurrent laryngeal nerve. The lower parathyroid glands originate
from the third pharyngeal arch, follow the long descent of the thy-
mus gland and, therefore, assume a great variety of possible posi-
tions. Ectopic positions can be localised from the carotid sheath
down to the pericardium. An ectopic position of the upper para-
thyroid gland is observed less frequently (20%).
Localisation diagnosis by ultrasound as the basis of minimal
invasive surgery for primary hyperparathyroidism (pHPT)
High-resolution ultrasonography is a highly sensitive procedure
for the preoperative diagnosis of parathyroid adenomas in pa-
tients with pHPT [12–14]. The common description of the para-
thyroid gland is a hypoechoic, sharply delineated, round to oval
node, close to the dorsal plain of the thyroid gland. This simplified
description of the ultrasound morphology of parathyroid glands
might decrease the rate of correct preoperative localisation diag-
nostics. Therefore, the scope of this overview is the demonstration
Fig. 1 Standard image of an oval hypoechogenic parathyroid gland
(8.5  7 mm).
Abb. 1 Typisches Bild einer ovalen, echoarmen Nebenschilddrse
(8,5  7 mm).
Fig. 2 Parathyroid gland with a hyperechogenic central region with
hypoechogenic halo (12.6  4.9 mm).
Abb. 2 Nebenschilddrse mit echoarmem Randsaum und zentral
echoreicherer Echotextur (12,6  4,9 mm).
Rewerk S et al. Morphological Features of … Ultraschall in Med 2006; 27: 256–261
Pictorial Essay
257

of ultrasound morphology differing from the most frequently ob-
served picture, which is the hypoechoic oval structure.
Echogenicity
In many cases, the parathyroid gland is positioned behind the
thyroid, oval in shape, with a hypoechoic pattern, when compared
to the neighboring tissue of the thyroid gland (Fig.1).
We have also observed reflex patterns of a parathyroid gland
which were isoechoic compared to the thyroid gland, with a hy-
poechoic margin (Fig. 2), which can make it difficult or even im-
possible to locate the parathyroid gland.
As shown in Fig. 3, the parathyroid gland, although 3 cm long, is
not revealed in the transcutaneous ultrasound due to isoechogeni-
city. Even in the intraoperative ultrasound examination, the differ-
ences in contrast were very low.
Outline
In approximately 30% of the cases, the enlarged parathyroid
glands did not have the features often described: oval outline in
Fig. 4
Transcutaneous ultrasound of a parathyroid gland with lobated
outline (max. 30  21.5 mm).
Abb. 4 Lobulierte Kontur einer Nebenschilddrse (max. 30  21,5 mm).
Fig. 3
Intraoperative ultrasound showing a very low contrast between
thyroid and parathyroid tissue. This parathyroid gland was not detected
by transcutenous ultrasound (29  21 mm).
Abb. 3 Intraoperativer Ultraschall mit geringem Kontrastunterschied
zwischen Schilddrse und Nebenschilddrse. Transkutan war die Neben-
schilddrse nicht darstellbar (29  21 mm).
Fig. 5aParathyroid gland with central cystic- regressive transforma-
tion (15  14.9 mm). b Operative specimen in midline transsection
showing regressive transformation as detected in ultrasound (cp.
Fig. 5a).
Abb. 5a Nebenschilddrse mit zentral zystisch-regressiver Transfor-
mation (15  14,9 mm). b Operationsprparat, mittig aufgeschnitten,
zeigt eine regressive Zone, wie im Ultraschall dargestellt (vgl. Abb. 5a).
Rewerk S et al. Morphological Features of … Ultraschall in Med 2006; 27: 256– 261
Pictorial Essay
258

combination with a hypoechogenic and homogeneous echotex-
ture. During our ultrasound examinations, we encountered a vari-
ety of shapes and outlines of the parathyroid gland. Oval contours
are shown in Fig.1, 2, and 7; lobated margins (Fig. 4) as well as
round outlines.
Echotexture
The echotexture of parathyroid glands often appears homoge-
neous, but small cystic-regressive inclusions exist, as well. Fig. 5a,
b show how the intraoperative impression of the dissected gland
parallels the transcutaneous sonomorphology.
Cystic-regressive changes can occupy as much as half of the vol-
ume of the parathyroid gland (Fig. 7). If there are multiple cystic-
regressive areas alongside hyperechoic areas within one halo, they
can be mistaken for a thyroid adenoma (Fig. 6).
Differential diagnosis
Thyroid nodules (Fig. 8) and malignant lymph nodes (Fig. 9) are
common differential diagnoses. Comparison of Fig. 8 and Fig. 6, 7
clearly demonstrates their similarity and the difficulty of differen-
tiating between them. Fig.10 displays the very rare case of an in-
trathyroidal metastasis of a renal cell carcinoma. There is little dif-
ference to an intrathyroidal parathyroid gland (Fig.12)
Fig. 6 Parathyroid gland with a halo, multiple regressive areas and
central hyperechogenic areas very similar to a thyroid adenoma. Com-
plete acoustic shadowing behind the clavicle, covering the lower part
of the gland (48  35 mm).
Abb. 6 Nebenschilddrse mit Halo, zahlreichen regressiv-echofreien
Zonen und zentral reflexreicheren Zonen, hnlich einem Schilddrsen-
adenom (48  35 mm).
Fig. 7 Parathyroid gland with an expanded regressive area
(22  16 mm).
Abb.7 Nebenschilddrse mit einer ausgedehnten regressiven Zone
(22  16 mm).
Fig. 8 Thyroid node as a differential diagnosis of a parathyroid gland
(20  30 mm), (cp. Fig. 7).
Abb. 8 Schilddrsenknoten als Differenzialdiagnose einer Neben-
schilddrse (20  30 mm), (vgl. Abb. 7).
Fig. 9 Lymphnode metastasis (22  20 mm) as a differential diagnosis
of a parathyroid gland.
Abb. 9 Lymphknotenmetastase (22  20 mm) als eine Differenzial-
diagnose einer Nebenschilddrse.
Rewerk S et al. Morphological Features of … Ultraschall in Med 2006; 27: 256–261
Pictorial Essay
259

Sonomorphology of parathyroid glands in secondary
hyperparathyroidism and MEN
Echogenity, outline, and echotexture of parathyroid glands in sec-
ondary hyperparathyroidism and MEN are quite similar to those of
adenomas in pHPT.
In contrast to primary hyperparathyroidism, however, more than
one parathyroid gland per field of vision is detectable in secondary
hyperparathyroidism, as a rule. In these cases, differences in out-
lines and dimensions are typical (Fig.11).
Since 5% of the patients have a fifth parathyroid gland, it is of ut-
most importance to actively look for it. A fifth gland located in-
trathyroidally (Fig.12) was overlooked in primary surgery, leading
to a reoperation that could have been avoided [6].
A noteworthy specialty is the riding position of the upper gland on
the lower one (Fig.13). Fig.14 shows the rare finding of three ipsi-
lateral parathyroid glands in a case of MEN1.
Conclusion
The pathologically enlarged parathyroid glands presented them-
selves in a great variety of guises as shown above. No malignant
transformation of a gland could be detected. A high level of experi-
ence is necessary to cope with the demanding challenge of pre-
operative localisation. This fact has been described earlier (1987)
Fig. 10 Intrathyroidal metastasis of a renal cell carcinoma
(40  29 mm), (cp. Fig. 12).
Abb. 10 Intrathyreoidale Metastase bei Nierenzellkarzinom
(40  29 mm), (vgl. Abb. 12).
Fig. 12 Hypoechogenic, hyperplastic, supernumerous parathyroid
gland, intrathyroidal at the lower pole of the thyroid gland
(17.7  17.4 mm).
Abb. 12 Echoarme hyperplastische, berzhlige Nebenschilddrse
intrathyreoidal im Schilddrsenunterpol (17,7  17,4 mm).
Fig. 11 Two parathyroid glands in one field of vision in a case of
secondary hyperparathyroidism (20  13 mm; 14,8  13,5 mm), no
thyroid pathology.
Abb. 11 Zwei Nebenschilddrsen in einem Schallfenster bei sekun-
drem Hyperparathyroidismus (20  13 mm; 14,8  13,5 mm), keine
Schilddrsenpathologie.
Fig. 13 Rare “riding position” of two ipsilateral parathyroid glands
(12  7 mm both glands together).
Abb. 13 „Reitende Position“ zweier seitengleicher Nebenschilddr-
sen (12  7 mm beide Drsen zusammen).
Rewerk S et al. Morphological Features of … Ultraschall in Med 2006; 27: 256– 261
Pictorial Essay
260

and is still unchanged [15]. Even if performed with 10-MHz
probes, the quality of the pictures presented was very poor at the
time [15]. Nowadays, modern ultrasound machines allow a much
more detailed view of the parathyroid glands, as demonstrated in
this essay. The knowledge of possible abnormal positions, varia-
tions in echogenicity, outline, and echotexture will lead to a highly
sensitive and specific ultrasound examination. The combination of
these findings with Sesta-MIBI-Scintigraphy will allow the sur-
geon to perform a minimal-invasive procedure in primary hyper-
parathyroidism, or a safe parathyroidectomy in secondary hyper-
parathyroidism or MEN.
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