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\title{Incidentally discovered parathyroid lipoadenoma in thyroid surgery: a
case report and review of the literature}



\author[1]{Yihan Wang}%
\author[1]{yan chen}%
\author[1]{Yantao Fu}%
\affil[1]{Jilin University}%


\vspace{-1em}



  
  \date{June 09, 2024}


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\textbf{1. Introduction}

Parathyroid lipoadenoma,one of the rare causes of primary
hyperparathyroidism, is an uncommon type of parathyroid adenoma,
described as a single parathyroid adenoma with more than 50\% fat on
histologic examination and an unknown etiology. There are currently 64
cases of parathyroid lipoadenoma reported on PubMed. We present a case
that supplements and supports the rare literature data concerning the
clinical and therapeutic aspects of occasional parathyroid lipoadenoma
in thyroid cancer surgery in our treatment centre and review the
relevant literature.

\textbf{2. Case Description}

The patient was a middle-aged male with a body mass index (BMI) of 38.4
who was hospitalized with thyroid nodules for 40 days. Physical
examination showed that the thyroid gland was firm and no obvious mass
was palpable; ultrasonography showed normal thyroid gland size,
heterogeneous glandular echoes, patchy hypoechoic areas, the larger one
was located in the right lobe, with a range of about 2.7 \selectlanguage{ngerman}× 1.09 cm, a
hypoechoic nodule was observed in the lower deep layer of the right
lobe, with a size of about 0.61 × 0.60 cm, aspect ratio \textgreater{}
1, regular borders, and punctate hyperechogenicity was observed; an
anechoic nodule was observed in the middle superficial layer, with a
size of about 0.28 × 0.34, aspect ratio \textless{} 1, regular borders,
and no significant focal hyperechogenicity was observed; a solid
hypoechoic nodule was observed in the lower grade of the left lobe, with
a size of about 0.54 × 1.01 cm, aspect ratio \textless{} 1, regular
borders, and no significant focal hyperechogenicity was observed. No
significant abnormal enlarged lymph nodes were found in bilateral neck.
Cytological examination of the right thyroid lobe nodule showed atypical
cells suggestive of papillary thyroid carcinoma. Thyroid function tests:
thyroid stimulating hormone TSH 0.862 mIU/L (normal reference value
0.372 -- 4.94 mIU/L); parathyroid hormone PTH 64.62 pg/ml (normal
reference value 15 -- 56 pg/ml); serum calcium Ca 2.42 mmol/L (normal
reference value 2.2 -- 2.65 mmol/L).

Resection of the right lobe and isthmus of the thyroid gland and central
lymph node dissection were planned, during which the right lobe and
isthmus of the thyroid gland were first removed, and grayish white
nodules were observed in the right lobe of the thyroid gland by
dissection, about 0.4 cm in diameter, and the remaining sections were
grayish red and soft.During the resection, two masses measuring 1.5 ×
0.8 × 0.7 cm and 2.5 × 1.5 × 0.5 cm were found in the dorsal and lateral
aspect of the middle and upper parts of the right lobe, respectively.The
texture was firm, the surface was smooth and the boundary was clear. The
possibility of parathyroid gland mass was considered, so it was decided
to remove the tissue for rapid pathological examination.The results
showed that round cells were scattered in the fibroadipose tissue of the
middle and upper dorsum of the right lobe, not excluding the mass of
parathyroid gland origin; most of the tissues submitted to the lateral
aspect of the middle and lower parts of the right lobe were fat, in
which a few round cells were scattered.At the same time, the left
thyroid gland was dissected to explore the tracheoesophageal groove of
the lower pole of the thyroid gland in its dorsal pole, and no abnormal
hyperplastic parathyroid tissue was observed.PTH values were 29.68 pg/ml
and 35.71 pg/ml at 15 and 30 minutes after tumor resection,
respectively, and serum calcium was 2.30 mmol/L on the first day after
surgery.Postoperative paraffin pathology (Fig. 1. ) revealed that the
superior dorsal mass and the middle and lower lateral mass in the right
lobe were consistent with parathyroid lipoadenoma, and
immunohistochemistry (Fig. 2. ) revealed PTH (+); CgA (+); SyN (-); CD56
(-); TTF-1 (-); Tg (-); Ki-67 (\textless{} 1\% +), and the right lobe of
the thyroid gland was papillary thyroid carcinoma 0.4 cm in diameter;
there was one lymph node metastasis in the central group, and the
diameter of the metastasis was 0.05 cm; the isthmus was nodular
goiter.Euthyrox 50 \selectlanguage{greek}μ\selectlanguage{english}g was orally administered daily after surgery.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

Fig. 1. Parathyroid adenoma, composed of \textgreater{} 50\% mature
adipose tissue, with principal cells arranged in nests between adipose
tissues. Hematoxylin-eosin staining magnification \selectlanguage{ngerman}× 20 (a), × 40 (b),
and × 100 (c).\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

Fig. 2. Immunohistochemical sections of parathyroid lipoma demonstrating
positive parathyroid hormone in the cytoplasm, magnified \selectlanguage{ngerman}× 100 (a) and ×
200 (b).

One month later, the patient came to our hospital for reexamination,
without perioral numbness of four extremities, TSH 1.30000 mIU/L; PTH
28.51 pg/ml; Ca 2.59 mmol/L. At present, the patient came to our
hospital for reexamination 9 months after operation, without related
symptoms.

\textbf{3. Discussion}

Parathyroid lipoadenomas are rare and are incidentally detected during
thyroid cancer surgery in this case. In this paper, 40 literatures with
''parathyroid lipoademona'' as search term on
PubMed\selectlanguage{english}\textsuperscript{{[}1,2,4,5, 7-42{]}} and 65 cases of
parathyroid lipoadenoma (including this case) were counted. After
excluding 18 cases with missing clinical data, 47 cases had complete
clinical data, including 30 females and 17 males, with a female-to-male
ratio of about 1.8:1, that is, parathyroid lipoadenoma accounted for a
higher proportion in females than in males. In addition, it has been
reported in the literature that parathyroid lipoadenoma may account for
a higher proportion in males than parathyroid adenoma
\textsuperscript{{[}1{]}}. The age of onset of parathyroid lipoadenomas
varies from 24 to 88 years, mostly located in the neck, but up to 15\%
of parathyroid lipoadenomas are ectopic or located in the mediastinum,
much higher than common parathyroid adenomas\textsuperscript{{[}2{]}}.

In 1958, Ober and Kaiser\textsuperscript{{[}3{]}} first described
parathyroid lipoadenoma in a middle-aged man with a gradually enlarging
neck mass that was painless and without manifestations of
hyperparathyroidism.A large lipoma was found under the sternum on neck
exploration.Because the tumor was nonfunctional, they named it
''parathyroid hamartoma''.The concept of ''parathyroid lipoadenoma'' was
first introduced in 1962 by Abul Haj \textsuperscript{{[}4{]}} et
al.Parathyroid lipoadenoma is a rare type of parathyroid adenoma with an
incidence of 0.5\% to 1.6\% of primary hyperparathyroidism and contains
fat, principal cells, and eosinophils, of which fat content is
\textgreater{} 50\%, unlike adenomas with fatty infiltration, and the
fat component is an integral part of parathyroid
lipoadenoma\textsuperscript{{[}5{]}}.In 2022, the World Health
Organization defined parathyroid lipoadenoma as ''a tumor with
simultaneous increases in parathyroid parenchyma and adipose tissue, and
more than 50\% of the glandular volume consists of adipose
tissue''\textsuperscript{{[}6{]}}.In the currently reported cases of
parathyroid lipoadenoma, the origin of the adipose tissue component is
unknown, and most of them are small brown lesions with the largest
reported weight of 480 g.Some researchers have speculated that the
factors of increased fat composition may be the same as those of
increased parathyroid chief cells \selectlanguage{english}\textsuperscript{{[}7,8{]}}.It has
been suggested that fat may be present in adenomas by high BMI, and some
speculations suggest that some adipogenic factors may be produced by
adenoma epithelial or stromal cells, which in turn stimulate adipocyte
proliferation\textsuperscript{{[}9{]}}.Christofer Juhlin proposed that
parathyroid lipoadenomas may be associated with
hypertension\textsuperscript{{[}5{]}}.

Parathyroid lipoadenomas can be classified as functional and
non-functional, with approximately 64 percent of previously reported
cases symptomatic, 28 percent asymptomatic, and 7 percent
suspicious\textsuperscript{{[}10,11{]}}, and four parathyroid
lipoadenomas found on autopsy for which function is uncertain. Among
them, the clinical features, laboratory tests and parathyroid adenomas
of functional parathyroid lipoadenomas are similar, that is, patients
show recurrent urinary stones and hip or shoulder fractures, but the
increase in parathyroid hormone and blood calcium may not be as obvious
as parathyroid adenoma, and a very small number of patients have
asymptomatic hypercalcemia.

The difficulty of parathyroid lipoadenoma is mainly diagnosed by
preoperative imaging localization.29 of 64 patients (45\%) had lesions
localized using imaging studies.Ultrasonography was performed in 24
cases, and lesions or suspected lesions were found in 14 (58\%) of
them.Computed tomography(CT) was reported in 12 cases, of which 9 (75\%)
detected or suspected lesions.Technicium-99m sestamibi scintigraphy was
reported in 15 cases, of which 8 (53\%) reported detection or suspicion
of lesions.In one of them, an X-ray was performed and the tumor was
found to be located in the mediastinal cavity.Positron emission
tomography (PET) scans were used in 6 cases, of which 3 (50\%) were
reported as lesions.Because of the high adipose tissue content, lipomas
tend not to be detected by preoperative imaging techniques.On
ultrasound, typical parathyroid adenomas are homogeneous hypoechoic
lesions, however, fat-rich variants of parathyroid adenomas sometimes
present as hyperechoic lesions \textsuperscript{{[}9{]}}, resulting in
reduced accuracy, and ultrasound examination of this patient showed no
parathyroid lesions; they can be localized as lipomatous masses on CT,
and Johnson et al\textsuperscript{{[}12{]}} reported cases in which CT
scans of parathyroid lipoadenomas had CT values of \selectlanguage{english}- 60 to \selectlanguage{english}- 90 HU,
consistent with lipoma density, proposing the possibility of parathyroid
lipoadenomas on such CT scans in similar cases of non-local primary
HPT.However, CT may also be confused with lipomas, lymph nodes, or other
fat-rich lesions; the accuracy of dual-phase Sestamibi scanning of the
parathyroid depends on the proportion of parathyroid chief cells, which
are more than 50\% fat in parathyroid lipoadenomas and have less
principal cell content than normal parathyroid tissue, resulting in
reduced accuracy of Sestamibi scanning; however, there are
cases\textsuperscript{{[}13{]}} indicating the usefulness of using
99Tcm-MIBI imaging in localizing the diagnosis, reoperation, and
persistent hyperparathyroidism, and they propose speculation that the
lesion may be shown based on the space-occupying appearance, or that the
target may have a low signal ratio to the background.Cases showed a good
target-background signal ratio in Tc-99m sestamibi imaging, which may be
due to the relatively large size of the lesion, as well as the fact that
the main part of the lesion consists of parathyroid chief cells; the
sensitivity of syngeneic SPECT for parathyroid lipoadenoma was
significantly reduced \textsuperscript{{[}12{]}}.However, Sabri et
al.\textsuperscript{{[}1{]}}concluded that although SPECT is not as
effective as parathyroid adenoma in the diagnosis of parathyroid
lipoadenoma, it may be superior to ultrasound.Cholinergic PET-CT imaging
is superior to ultrasound and CT in the localization of parathyroid
adenoma, but there is no relevant report for parathyroid lipoadenoma.

Primary hyperparathyroidism is most commonly caused by solitary
parathyroid adenomas, accounting for more than 80 -- 85\%; less
commonly, parathyroid hyperplasia, parathyroid carcinoma, and multiple
parathyroid adenomas\textsuperscript{{[}2{]}}. Parathyroid lipoadenoma
is a very rare cause of primary hyperparathyroidism with an incidence of
0.5\% to 1.6\% of primary hyperparathyroidism. In parathyroid
lipoadenomas, the sensitivity of imaging is significantly reduced by low
parathyroid cell concentration and excessive fat content. Abundant
adipocytes in parathyroid tissue can be found in the following
conditions: normal tissue, lipohyperplasia, lipoadenoma, and cancer
infiltrating the surrounding adipose tissue. It is difficult to
differentiate these diagnoses by intraoperative rapid frozen section.
Therefore, definitive diagnosis of parathyroid lipoadenoma should
include pathologic diagnosis of parathyroid hyperplasia within adipose
tissue, as well as a significant decrease in hormone following
intraoperative removal of the parathyroid gland. Increases in
parathyroid gland weight (\textgreater{} 40-60 mg) may also represent
parathyroid lipoadenomas in appropriate morphologic and clinical
settings \textsuperscript{{[}6{]}}. Parathyroid lipoadenomas should be
considered when no lesions are reported on ultrasound but clearly
identified by CT or SPECT. Parathyroid carcinoma infiltrating in adipose
tissue may be misdiagnosed as parathyroid lipoadenoma, so careful
pathological examination is still required for differential diagnosis.

\textbf{4. Conclusions}

Parathyroid lipoadenoma is a rare cause of primary hyperparathyroidism,
which is mainly manifested as infiltration of a large amount of adipose
tissue in the gland, and due to excessive fat content, its sensitivity
in imaging localization diagnosis is reduced, and the difficulty of
parathyroid lipoadenoma is still in preoperative localization diagnosis,
so we believe that parathyroid lipoadenoma needs to rely on paraffin
pathology to make a final diagnosis.This case report serves as a
reminder that patients with preoperative unprovoked primary
hyperparathyroidism and negative imaging findings may have a parathyroid
lipoadenoma. During intraoperative thyroidectomy or lymph node
dissection, it is important to carefully examine the adipose tissue for
the possibility of parathyroid lipoadenoma, as this can lead to
postoperative hypoparathyroidism or even intractable hypocalcemia.

\textbf{Declarations}

\textbf{Ethical Approval:}

The authors are accountable for all aspects of the work in ensuring that
questions related to the accuracy or integrity of any part of the work
are appropriately investigated and resolved. All procedures performed in
this study were in accordance with the ethical standards of the
institutional and/or national research committee(s) and with the
Helsinki Declaration (as revised in 2013). Written informed consent was
obtained from the patient for publication of this case report and
accompanying images. A copy of the written consent is available for
review by the editorial office of this journal.

\textbf{Competing interests:}

The authors have no conflicts of interest to declare.

\textbf{Authors' contributions:}

(I) Conception and design: Yihan Wang

(II) Administrative support: Yantao Fu

(III) Provision of study materials or patients: Yantao Fu

(IV) Collection and assembly of data: Yihan Wang

(V) Data analysis and interpretation: Yihan Wang

(VI) Manuscript writing: All authors

(VII) Final approval of manuscript: All authors

\textbf{Funding:}

No

\textbf{Availability of data and materials:}

In this paper, 40 literatures with ''parathyroid lipoademona'' as search
term on PubMed and 65 cases of parathyroid lipoadenoma (including this
case) were counted.

This case comes from the Department of Thyroid Surgery, China-Japan
Union Hospital of Jilin University, we do not wish to share the data for
the sake of patient privacy protection principles.

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