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The Journal of Clinical Endocrinology & Metabolism 89(7):3208 –3213
Copyright © 2004 by The Endocrine Society
doi: 10.1210/jc.2003-031184
Weight of Normal Parathyroid Glands in Patients with
Parathyroid Adenomas
KATHY YAO, FREDERICK R. SINGER, SANFORD I. ROTH, AARON SASSOON, CYNTHIA YE,
ARMANDO E. GIULIANO
AND
Department of Breast and Endocrine Disease, John Wayne Cancer Institute at Saint John’s Health Center (K.Y., F.R.S.,
C.Y., A.E.G.), Santa Monica, California 90404; Department of Pathology, Harvard Medical School and Massachusetts
General Hospital (S.I.R.), Boston, Massachusetts 02114; and Department of Pathology, Saint John’s Health Center (A.S.),
Santa Monica, California 90404
Although the size and weight of a parathyroid gland are frequently the only intraoperative determinants of abnormality,
these parameters have not been examined in living patients
with primary hyperparathyroidism (PHP). The records of 240
patients who underwent parathyroidectomy according to
standard surgical practice by a single surgeon were reviewed
to identify those who were euparathyroid after in toto removal of a histologically confirmed normal gland and a histologically confirmed adenoma. The 25 (86%) females and 4
(14%) males who met the study criteria had a mean age of 60
yr (range, 33– 82 yr). The mean PTH level was 130.1 pg/ml
(range, 58 –278) before parathyroidectomy and 32.4 pg/ml
(range, 1– 68) after parathyroidectomy. The mean calcium
level was 11.1 mg/dl (range, 10 –14) before and 8.7 mg/dl (range,
C
ORRECT INTERPRETATION OF parathyroid gland
pathology intraoperatively has always been the cornerstone of successful parathyroidectomy for the treatment
of primary hyperparathyroidism (PHP) (1–3). To distinguish
between an adenoma and primary chief cell hyperplasia in
nonfamilial and nonmultiple endocrine neoplasia-associated
PHP, the surgeon often relies on gland size and shape and
the proper pathological interpretation by the pathologist using frozen sections (2). The intraoperative diagnosis affects
surgical management; primary chief cell hyperplasia is
treated by subtotal parathyroidectomy, whereas an adenoma
is managed by removal of a single gland and identification
of a normal gland (2). Recent studies using radiographic
scanning rely on identification of abnormal glands by sestamibi labeling, intraoperative PTH measurement, sonography, and/or magnetic resonance imaging and have led to the
use of minimally invasive surgical techniques without identifying the normal glands (4). The accuracy of these methods
is to some extent dependent upon the fact that almost 85%
of the nonfamilial, nonmultiple endocrine neoplasia patients
have single adenomas (Table 1).
Gross distinction between normal glands and small hyperplastic glands requires an experienced parathyroid surgeon and pathologist. Weight and size are the most frequently used criteria; the shape of the gland also can be
Abbreviation: PHP, Primary hyperparathyroidism.
JCEM is published monthly by The Endocrine Society (http://www.
endo-society.org), the foremost professional society serving the endocrine community.
8 –10) after parathyroidectomy. Thirty-four intact normal
glands were removed and available for analysis. Their mean
weight was 62.4 ⴞ 31.6 mg (range, 18 –161 mg), and 15 (44%)
weighed 60 mg or more. The mean weight of the adenomas was
553.7 ⴞ 520.5 mg (range, 66 –2536). Adenomas were clearly distinguished from normal glands by cellularity, stromal fat, and
intracellular fat in chief cells. The weight of normal parathyroid glands removed at surgery in patients with PHP may be
greater than that reported in autopsy studies. Therefore, certain histological features are a better measure than weight in
determining whether a gland is normal, and intraoperative
identification of slightly enlarged glands should not lead to
immediate subtotal parathyroidectomy. (J Clin Endocrinol
Metab 89: 3208 –3213, 2004)
useful (3). The density of pieces of the gland has been
proposed to distinguish between normal and abnormal
parathyroid glands (5, 6). Histological examination to determine cellularity and the amount/distribution of stromal and intracellular fat (7) is used to confirm the gross
impression.
The reported weights of normal parathyroid glands are
based on autopsy studies of subjects who did not have PHP
(Table 2) (8 –13). Only one antemortem study has examined
the weights of parathyroid glands. The study included patients with normocalcemic hyperparathyroidism, and some
of the patients had parathyroid hyperplasia (14, 15). In the
present study we identified a group of patients who had total
surgical resection of a histologically normal parathyroid
gland in conjunction with resection of a histologically confirmed adenoma. In contrast to other studies examining normal parathyroid weights, these patients all had a diagnosis
of PHP before surgery, and their parathyroid glands were
weighed after dissection to remove capsular fat and thymic
tissue in the operating room. Independent histopathological
examination by three pathologists and clinical follow-up excluded cases of primary chief cell hyperplasia.
Subjects and Methods
The records of 240 patients who underwent parathyroidectomy by a
single surgeon for PHP between 1998 and 2002 were reviewed. Patients
undergoing parathyroidectomy for secondary or tertiary hyperparathyroidism, primary parathyroid hyperplasia, or parathyroid carcinoma;
patients without an entire apparently normal parathyroid gland to evaluate; and patients with apparent adenoma whose postoperative serum
chemistries did not normalize were excluded from the study. The study
3208
Yao et al. • Weight of Normal Parathyroid Glands
J Clin Endocrinol Metab, July 2004, 89(7):3208 –3213 3209
TABLE 1. Causes of PHP in 3131 cases treated at Massachusetts
General Hospital between 1930 and 2003 (Roth, S. I., unpublished
data)
Cause
No. of cases (%)
Adenoma
Single
Double
Hyperplasia
Clear cell
Chief cell
Carcinoma
2640 (84.3)
2506 (83.0)
38 (1.2)
457 (14.6)
20 (0.6)
437a (14.0)
34 (1.1)
Total
3131
TABLE 3. Pre- and postoperative serum PTH and calcium levels
for 29 patients who underwent parathyroidectomy
No. of
patients
Mean (range)
P value
29
27
130.1 (58 –278)
32.4 (1– 68)
⬍0.0001
29
29
11.1 (10 –14)
8.7 (8 –10)
⬍0.0001
PTH (pg/ml)a
Before operation
After operation
Calcium (mg/dl)
Before operation
After operation
a
Postoperative levels available for 27 of 29 patients (normal range,
10 – 65 pg/ml).
a
Includes 41 familial and multiple endocrine neoplasia patients
(1.4% of all patients).
TABLE 2. Autopsy studies on weight of normal parathyroid
glands in patients without PHP
Year
No. of
cases
Gilmour and Martin (8)
1937
428
Wang (9)
Dekker et al. (10)
Akerstrom et al. (11)
Ghandur-Mnaymneh et al. (12)
1976
1979
1981
1986
160
33
503
166
Study
Mean weight of
normal glands
(mg)
29.4 (males)a
32.8 (females)a
35– 40b
29.9 ⫾ 15.1
31 ⫾ 16
39.5 ⫾ 20.8
a
Average weight of a single gland calculated from a combined
four-gland weight.
b
Average weight range.
group included only those patients in whom an intact, histologically
normal gland was removed in addition to one or two adenomas. The size
of the normal gland, as assessed intraoperatively or on pathological
evaluation, was not used as an inclusion criterion. Patients who underwent biopsy or partial removal of a normal gland were excluded, because the normal gland weight could not be accurately determined. Of
the 240 cases, 62 initially appeared to meet the inclusion criteria in which
a single adenoma was removed in conjunction with in toto removal of
a normal parathyroid gland. After review of the histological slides and
the medical records by two pathologists independently, it appeared that
41 of these 62 cases fulfilled the criteria for the study. That is, the
removed tissue included an apparently histologically normal parathyroid gland removed in toto and an abnormal gland, and the patient
became euparathyroid postoperatively. The remaining 21 cases were
excluded because they were determined to be primary chief cell hyperplasia or did not demonstrate a euparathyroid state on further postoperative follow-up. The 41 cases were then reviewed by a third pathologist (S.I.R.), and 12 additional cases were excluded, leaving 29 patients.
Three cases were excluded because no abnormal gland was present
histologically, one case had no normal gland, and seven cases were
diagnostic of primary chief cell hyperplasia (1, 3). One patient had a
double adenoma. The 29 cases exhibited normalization of serum PTH
and calcium levels postparathyroidectomy (Table 3). The surgeon’s assessments of the size of the normal gland were recorded intraoperatively
as normal, slightly large, or large, but these assessments were not used
as inclusion criteria for the study. Adenoma weights or histology, clinical
features, or preoperative biochemical findings were not significantly
different between the excluded and nonexcluded patients.
Nineteen patients had undergone preoperative localization studies
with sestamibi scanning. Intraoperative PTH monitoring was performed
on only one of the patients and was not used as a criterion for successful
parathyroidectomy in this study.
This study was reviewed and approved by the institutional review
board of Saint John’s Health Center, and informed consent was waived
due to the retrospective nature of the study.
Histological assessment
A gland was identified as histologically normal by the following
criteria: the presence of abundant stromal fat occupying greater than
50% of the stroma and impinging upon the parathyroid epithelial cells
(chief and oxyphil cells), which are arranged in a branching trabecular
pattern, and the presence of abundant intracellular fat in the chief cells
(1, 3, 7, 13, 16). Oxyphil cell nodules were present in some normal glands.
A gland was identified as abnormal by the predominance of epithelial
cells, chief cells, oxyphil cells, or a mixture of cell types in a variable
cellular pattern; a paucity of stromal fat in an irregular distribution; and
diminished intracellular fat (1, 3, 7). The epithelial cells were distributed
in sheets, cords, and follicles, and in the focal areas of stromal fat the
epithelial cells appeared to impinge upon the stromal adipose cells.
These two features establish the diagnosis of parathyroid adenoma. A
so-called rim of normal tissue outside the adenoma capsule is not considered a valid criterion for diagnosing an adenoma, because pseudonormal glandular tissue not separated from the adenoma by a capsule
is quite common around both adenomas and glands with primary chief
cell hyperplasia (1, 3).
Results
Our study group thus comprised 29 patients. The mean
age of the 29 patients was 60 yr (range, 33– 82 yr). All but four
(14%) were female. Sixteen patients (55%) had a symptomatic
clinical presentation. As shown in Table 3, serum PTH and
calcium levels significantly returned to normal after parathyroidectomy (by paired t test, P ⬍ 0.0001).
Twenty-five patients had one normal parathyroid gland
removed, three patients had two normal glands removed,
and one patient had 2.75 normal glands removed. The mean
weight of the 34 normal glands was 62.4 ⫾ 31.6 mg (range,
18 –161 mg); 15 normal glands weighed at least 60 mg, including three more than 100 mg. Twelve normal glands
weighed between 40 and 59 mg, and the other seven normal
glands weighed between 18 and 39 mg (Fig. 1A). The mean
weight of 25 normal glands, after excluding the four patients
with two or more normal glands, was 54.9 ⫾ 28.6 mg (range,
18 –152 mg). The mean weight of 29 adenomas was 553.7 ⫾
520.5 mg (range, 66 –2536 mg; Fig. 1B). Most adenomas were
in the right inferior position; normal glands were evenly
distributed between the right inferior and left superior
positions.
By surgical assessment, all adenomas were large or slightly
large, but 76% of normal glands were large or slightly large,
which explains why a whole normal gland was removed in
these cases. Dimensions were 6 –30 ⫻ 5–15 ⫻ 3– 8 mm for
adenomas and 3–10 ⫻ 2– 6 ⫻ 2– 4 mm for normal glands.
Of the 19 patients who underwent preoperation localization studies with sestamibi scanning, none had a normal
3210
J Clin Endocrinol Metab, July 2004, 89(7):3208 –3213
FIG. 1. A, Graph shows weights of 34 normal parathyroid glands in
29 patients with PHP. B, Graph shows weights of 29 adenomatous
glands in 29 patients with PHP.
gland removed as a consequence of high radioactive counts
intraoperatively.
Multivariate analysis (repeated measurement using a
mixed model) failed to identify any correlation between the
weight of normal parathyroid glands and the patient’s
weight, body mass index, age, or gender.
Discussion
We examined the weights of 34 histologically normal parathyroid glands that were removed from 29 patients with PHP
because these glands were grossly enlarged. The average
weight of these glands was considerably greater than the
weight of normal glands reported in the literature; 15 glands
weighed at least 60 mg. Most surgeons and pathologists
consider a weight of 60 mg or more in the setting of another
enlarged gland to be indicative of primary chief cell hyperplasia or, rarely, a double adenoma. Our study group included only those patients whose adenomas had been confirmed by histological and clinical assessment. Independent
review confirmed the histological evaluation, and all study
patients demonstrated normalization of their serum calcium
and PTH levels after surgery. It should be noted that not all
surgical pathologists might agree with our judgment that the
enlarged glands were normal. In the absence of physiological
and molecular studies, only long-term (years) follow-up
would definitively prove our diagnosis, because primary
Yao et al. • Weight of Normal Parathyroid Glands
chief cell hyperplasia may recur as late as 10 –12 yr after
surgical removal of one or two glands (Roth, S. I., unpublished observations). It is important to note that these cases
were included in the study based on histological criteria and
not on the gross size of the gland. Those glands characterized
by stromal fat that occupied greater than 50% of the stroma
and compressed the parenchymal cells and by increased
intracellular fat in the chief cells were considered normal.
These histologically normal glands were removed because
they appeared larger than the other glands and therefore
were considered suspicious for adenoma. This practice is
considered the surgical standard of care for this disease process, and patients are made aware of the fact that normal
glands may be inadvertently removed during the consent for
parathyroidectomy. This selection bias for removal of larger
than normal glands makes it impossible for us to determine
the true incidence of high weight normal glands; nonetheless, this report demonstrates that high weight normal glands
do exist in some patients with PHP.
This paper is, to the best of our knowledge, the first to
examine the weights of normal parathyroid glands removed
during primary exploration in patients with PHP. All previous studies used postmortem specimens, usually from
patients without PHP (8 –12). An antemortem study was
published in 1976 (14, 15), but 46% of the patients had hyperplasia, and 23% had adenoma. The mean weight of 26
normal glands in that study was 36.5 mg; however, more
than half of the 26 cases recurred. It is not clear whether these
cases were missed double adenomas or, in fact, hyperplasia.
Gilmour and Martin’s classic study (8) from 1937 examined the weights of parathyroid glands in 428 autopsy cases.
The mean weight for all four normal parathyroid glands was
117. ⫾ 4.0 mg in males and 131.3 ⫾ 5.8 mg in females.
Dividing these numbers by 4 yields individual gland weights
of 29.4 mg for males and 32.8 mg for females. In 1976, Wang
(9) studied the location, size, weight, and shape of 645 normal
glands from 160 cadavers. He reported an average weight of
35– 40 mg; the largest gland weighed 78 mg. Glands tended
to be heavier in men between 20 and 30 yr of age and lighter
in women and the elderly (70 – 80 yr old). An autopsy study
published in 1979 analyzed normal parathyroid glands in 33
patients, none of whom had endocrine abnormalities (10).
More than three quarters of the glands had less than 30%
stromal fat, but 75% of the glands weighed less than 31 mg.
The researchers concluded that decreased stromal fat does
not necessarily imply hyperplasia. A Swedish study of 503
autopsy cases without parathyroid disease reported parathyroid weights of 31 ⫾ 16 mg (11). The fat content of the
glands reflected the general fat tissue content of the body.
The researchers concluded that the fat content of the parathyroid glands was not a reliable histological criterion and
that parenchymal cell weight should be used instead to differentiate normal glands from diseased glands. The most
recently published autopsy study examined weights of parathyroid glands in two groups: 100 healthy subjects whose
sudden death prompted investigation by the medical examiner and 66 patients with a spectrum of diseases that did not
include renal disease or hyperparathyroidism (12). The mean
weights of the glands were 39.5 ⫾ 20.8 and 46.2 ⫾ 23 mg for
the two groups, respectively; the glands tended to be heavier
Yao et al. • Weight of Normal Parathyroid Glands
FIG. 2. A, Photomicrograph of a normal parathyroid gland
from a patient with a parathyroid adenoma. The extensive
stromal fat is surrounded by cords and thin sheets of chief
cells. Small accumulations of oxyphil cells are seen interspersed among the chief cells. The stromal fat cells appear
to be compressing the parenchymal cells. Hematoxylin and
eosin stain was used. Original magnification, ⫻16. B, Photomicrograph of a small adenoma with an area of abundant
stromal fat at one edge. The parenchymal cells appear to be
compressing the stromal fat. Hematoxylin and eosin stain
was used. Original magnification, ⫻16. C, Photomicrograph
of a portion of a parathyroid adenoma without stromal fat.
The neoplastic cells are largely chief cells with interspersed
nodules of oxyphil cells. Hematoxylin and eosin stain was
used. Original magnification, ⫻16.
J Clin Endocrinol Metab, July 2004, 89(7):3208 –3213 3211
3212
J Clin Endocrinol Metab, July 2004, 89(7):3208 –3213
in the group with a spectrum of diseases. There was a slight
correlation between gland weight and body weight in both
groups. If we compare the mean weight (62.4 ⫾ 31.6 mg) in
our patients with PHP with that in the healthy subjects
(39.5 ⫾ 20.8 mg) without PHP, we find that our weights are
heavier by approximately 50%.
The main differential diagnosis during parathyroid surgery for PHP is between an adenoma and primary chief cell
hyperplasia. Table 1 shows the etiology of 3131 cases of PHP
treated at Massachusetts General Hospital since 1930 (Roth,
S. I., unpublished observations). Most (84.3%) patients had
adenomas. The smallest clinically documented adenoma was
50 mg (compared with 66 mg in our study); most adenomatous and hyperplastic glands weighed at least 100 mg.
It is not possible to distinguish between an adenoma and
primary chief cell hyperplasia on the basis of a single gland
by gross, microscopic, or ultrastructural features. An adenoma is identified by comparison with at least one normal
gland, and primary chief cell hyperplasia is diagnosed by
identifying abnormal histological features in at least three
glands. The classic features distinguishing an adenoma from
a normal gland are size, shape, consistency, and histological
features. Adenomas have grossly rounded blunt edges and
an increase in consistency, whereas normal glands have relatively sharp edges and a softer, more pliable consistency.
Microscopically, the normal glands in adults have an increased stromal fat content and increased intracellular fat in
the chief cells, compared with abnormal glands. Although
there may be stromal fat in abnormal glands, the fat is being
compressed by the parenchymal cells (Fig. 2, A and B),
whereas in the normal glands the fat appears to be compressing the parenchymal cells (Fig. 2C). Nonetheless, the
gold standard that distinguishes normal from abnormal
glands remains the histological features. Perhaps a physiological measure should replace histological criteria to distinguish abnormal glands (17). The most readily available
physiological test in use these days is intraoperative PTH
monitoring; unfortunately, this was available for only one of
the patients, and therefore, the results were not used in this
study. In this one patient, a drop in the PTH level was seen
after removal of the adenoma, but not the normal gland.
Immunohistochemistry has been used to identify vitamin D
receptor expression to distinguish adenomas from normal
glands (18), but this modality is only available at a limited
number of institutions and is not performed intraoperatively.
At this time we are still reliant on histomorphological features of the gland to help determine whether a gland is
hyperfunctioning.
Fat stains (Sudan IV or Oil Red O) have been used to
distinguish between normal and adenomatous glands. The
theory is that 80% of the cells in normal glands are in the
resting phase and contain abundant intracytoplasmic fat.
Hyperfunctioning glands should be hypercellular with little
or no fat. The fat stain can be helpful, but its accuracy is only
80%; it therefore should be used in conjunction with other
standard pathological criteria (7, 16, 19, 20).
Although 50 mg is often considered the upper limit of
normal parathyroid weight, 15 of the 34 glands in our study
weighed at least 60 mg; three glands weighed more than 100
mg. All 15 glands displayed gross histological characteristics
Yao et al. • Weight of Normal Parathyroid Glands
of normal glands; the glands had relatively sharp edges
grossly, and histologically the abundant stromal fat content
was impinging upon the parenchymal cells. These findings
suggest the importance of considering the consistency of the
gland and the relationship between stromal fat and parenchymal cells when determining whether a gland is abnormal.
If enlarged glands are otherwise normal, removal of 3.5 parathyroid glands could increase the chances of postoperative
hypoparathyroidism. When there is an obvious size discrepancy intraoperatively, asymmetric parathyroid hyperplasia
must be considered. However, because we have documented
three normal glands weighing as much as 100 mg, we believe
that removal of 3.5 glands should not be undertaken until
histological frozen section examination of two completely
resected glands has confirmed hyperplasia. This should reduce the incidence of postoperative hypoparathyroidism.
Furthermore, we have reported that selective subtotal parathyroidectomy for sporadic primary multiple gland disease
that leaves approximately 100 mg gland results in long-term
normocalcemia in 92% of cases (21).
In addition to strict histological criteria that differentiate
normal from abnormal, we used a significant postoperative
drop in PTH level and a normalization of the serum calcium
level to confirm the diagnosis. Although long-term outcome
assessment was not part of this study, unpublished data from
the Massachusetts General Hospital experience (Roth, S. I.,
May 2003) and other studies (22) indicate that a limited
number of patients who undergo apparently curative parathyroidectomy will develop recurrence within 10 yr. Thus,
we cannot exclude the possibility of recurrent hyperparathyroidism in our study population.
There are no published studies with which our results can
be compared. Because we found no correlation between the
normal gland weight and the patient’s weight, body mass
index, age, or gender, we can offer no physiological explanation for the preponderance of morphologically large normal glands. However, we can caution against overreliance on
gland size as an intraoperative indicator of disease. In addition, double adenomas are rare, comprising approximately
1% of all cases of PHP. Because grossly large glands may be
microscopically normal, the extent of resection should not be
determined merely by intraoperative size. Indeed, in our
study 79% of the normal glands were assessed as slightly
large or large in size by the surgeon, but normal based on
histological criteria by the pathologists. Intraoperative frozen
section can help determine whether larger glands are abnormal, but it is often unreliable because of artifacts from
processing and because only one part of the gland is examined if it is biopsied and not completely excised. Parathyroidectomy to remove 3.5 glands should not be considered
unless all glands are large and histological abnormalities are
detected that are confirmed by the pathologist to be due to
primary chief cell hyperplasia.
Acknowledgments
Received July 8, 2003. Accepted March 18, 2004.
Address all correspondence and requests for reprints to: Armando E.
Giuliano, M.D., John Wayne Cancer Institute, 2200 Santa Monica Boulevard, Santa Monica, California 90404. E-mail: [email protected].
Yao et al. • Weight of Normal Parathyroid Glands
This work was supported by funding from the Eli and Edythe L.
Broad Foundation (Los Angeles, CA) and Lois Rosen.
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JCEM is published monthly by The Endocrine Society (http://www.endo-society.org), the foremost professional society serving the
endocrine community.