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Table 20.1. Development and evolution of surgical treatment of primary hyperparathyroidism
Unilateral neck
Development Bilateral neck exploration
1920s
1930s
1940–60s
1970s
1980s
1990s
2000s
NIH: National Institute of Health
Mandl F: First successful
operation in Austria.
Mandl F: Recurrence of
the first case
Cope O: Successful
removal of a adenoma in
the mediastinum after
several failed neck
explorations
Ultrasonography
Computerized
tomography
A density test of resected
tissue
High-resolution
ultrasonography
201
99m
Tl-
Tc subtraction
scan
oil-red-O staining of
frozen sections
NIH Consensus for
asymptomatic cases
99m
Tc-sestamibi scan
intraoperative quick PTH
measurement
Prospective studies of
unilateral neck
exploration
Randomized controlled
trials of bilateral versus
unilateral or focused neck
exploration
Walton AJ: ‘‘always exposure all
the parathyroid glands,
sometimes search behind the
trachea and the
mediastinum’’
Kaplan EL: ‘‘strongly recommend
a bilateral exploration for all
patients’’
Proye CAG: ‘‘routine bilateral
neck exploration is
recommended’’
exploration
Wang CA: ‘‘only if an
adenoma is found on
the first side and the
other gland is
normal’’
Tibblin S: ‘‘it is not
necessary to explore
all four glands’’
Russell DFJ: ‘‘scan-
directed unilateral
neck exploration is a
legitimate
alternative’’
280
ENDOCRINE SURGERY
Focused
parathyroidectomy
Irvin GL: limited
parathyroidectomy
guided by
intraoperative quick
PTH measurement
Gagner M: endoscopic
parathyroidectomy
especially when excessive biopsies of normal
glands were performed [12]. In the survey
by Tibblin, surgeons were rather conservative
in intraoperative evaluation of normal-sized
parathyroid glands, and only nine respondents
performed the classical procedure among
43 surgical departments where bilateral neck
exploration was routinely performed [10]
(Table 20.2). Thus it is important to note
that what ‘‘bilateral neck exploration’’ means
may differ among endocrine surgeons with
regard to the extent of intraoperative evaluation techniques and the use of preoperative
localization tests.
281
PARATHYROID
Table 20.2. Questionnaire survey on surgical procedures for primary hyperpar-
athyroidism due to single parathyroid adenoma reported in 1991
Neck exploration Biopsy of normally appeared glands Respondents
Bilateral Excisional biopsy of one gland 7 (13%)
Incisional biopsy of three glands 9 (17%)
Incisional biopsy of one to two glands 16 (31%)
No biopsy 11 (21%)
Unilateral Excisional biopsy 6 (12%)
Incisional biopsy 3 (6%)
52 (100%)
Source: Data from [10].
Bilateral Versus Unilateral
Neck Exploration:
The Evidence
Systematic Review
Reeve et al. conducted a systematic review of the
literature to compare the outcomes of minimally invasive surgery (either unilateral or
focused) with those of bilateral neck exploration
[13]. The authors, however, faced difficulty in
drawing solid conclusions for the efficacy and
safety of minimally invasive surgery because the
selected studies differed in study designs, study
populations, preoperative localization tests,
surgical interventions, and outcomes [13–22]
(Table 20.3).
Prospective, Quasi-Experimental
Studies
Based on a prospective, multicenter study where
five different surgical regimens for patients with
primary hyperparathyroidism due to solitary
adenoma were compared, Tibblin and his
colleagues found that severe postoperative
hypocalcemia was significantly more common
after bilateral than unilateral exploration [23]
(Table 20.4). They also concluded that unilateral
parathyroidectomy without contralateral inspection were no more likely to cause persistent
or recurrent hypercalcemia than bilateral
approach, given the diagnosis of single gland
disease was confirmed by the use of intraoperative
fat staining. Other five prospective studies
on unilateral neck exploration (not focused
approaches) are summarized in Table 20.5.
Russell and his colleagues pioneered in adopting
the scan-directed unilateral neck exploration
where contralateral side was also explored if
preoperative
or the unilateral approach failed to identify the
parathyroid lesion [24]. Of the 90 patients in
the study, 48 (53%) had unilateral surgery while
the rest actually needed bilateral exploration.
Among 46 patients with unilateral approach
whose data were available at mean follow-up of
16.8 months, no one demonstrated persistent or
recurrent hypercalcemia. Since hypercalcemia did
not resolve in 6 of 42 individuals undergoing
bilateral exploration, the overall success rate of
this strategy was 93%. Later, the investigators
retrospectively reviewed the long-term outcome
of 184 patients in whom cervical exploration was
limited to one side [25]. Following the initial
operation three patients (1.6%) demonstrated
persistent hypercalcemia while none of the cured
patients had developed recurrent disease at mean
follow-upof59months.WeiandBurkeexamined
if preoperative radiologic localization with unilateral neck exploration reduced operative time
compared with full bilateral neck exploration.
They observed that unilateral neck exploration
provided 100% cure and would save approximately 30 min in completing curative surgery
[21]. Norman et al. also reported 100% cure
rate of unilateral neck exploration with a study
population of primary hyperparathyroidism
patients with a solitary adenoma detected by preoperative
201
99m
Tl-
Tc scanning was negative
99m
Tc sestamibi scanning [17]. Carty
ENDOCRINE SURGERY
Table 20.3. Studies included in the systematic review of unilateral and bilateral neck exploration for primary
hyperparathyroidism
Author Study design Study population Preoperative imaging Intervention Outcomes
Vogel [14] Retrospective 106 PHPT US (93), MIBI (17) UNE > BNE IS, OT, OS, AE
Denham [15] ‘‘meta-
analysis’’
Ryan [16] ‘‘Case-
100 sporadic PHPT US (93), Tl-Tc (84) UNE versus BNE IS, OT, OS, AE
control’’
Norman [17] Prospective
(with
historical
18 PHPT with MIBI positive
(25 PHPT as historical
controls)
MIBI (18) vs no tests
(25)
UNE versus BNE IL, OT, HS,
controls)
Vroonhoven [18] Prospective 66 PHPT US and CT Minimal > BNE OT, OS, AE
Tsukamoto [19] Not declared. 160 PHPT Tl-Tc UNE > BNE IS, OT, OS
Petti [20] Retrospective 100 PHPT Tl-Tc (50) vs. no tests
UNE versus BNE OT, OS, AE, C,
(50)
Wei [21] Prospective 33 PHPT with MIBI positive
indicating a solitary
adenoma.
MIBI UNE +
contralateral
neck
exploration
Worsey [22] Retrospective 371 sporadic PHPT US (22), Tl-Tc (24),
UNE > BNE OS, OT, AE
both (29), no tests
(275)
PHPT: primary hyperparathyroidism, MIBI:
tomography, UNE: unilateral neck exploration, BNE: bilateral neck exploration, UNE > BNE: unilateral neck exploration followed by contralateral
exploration if no enlarged parathyroid glands were identified on the first side, IS: imaging success, OT: operative time, OS: operative success, C:
cost, HS: hospital stay, AE: adverse event, IL: incision length, P: pathology.
Source: Data from [13].
99m
Tc-sestamibi scan, Tl-Tc:
201
99m
Tl-
Tc subtraction scan, US: ultrasonography, CT: computed
Performance
of MIBI
OT, C, P
OS, AE
HS
OT
282
Table 20.4. Prospective multicenter study comparing five surgical regimens for primary hyperparathyroidism
Outcome
hypercalcemia/
Study population
325 patients undergoing
initial Surgery for
primary
hyperparathyroidism
due to solitary adenoma
Preoperative
imaging
not described. 1. Unilateral PTX after UNE (50)
Intervention (number of available patients at
follow-up)
2. Unilateral PTX after BNE (44)
3. BNE with removal of the enlarged gland and
incisional biopsy of 1–2 normal-sized glands (84)
4. BNE with removal of the enlarged gland and
normocalcemia/
hypocalcemia (%)
2/96/2%
3/90/7%
11/80/9%
3/92/5%
incisional biopsy of 3 normal-sized glands (37)
5. BNE with removal of the enlarged gland but no
0/98/2%
biopsy (57)
PTX: parathyroidectomy, UNE: unilateral neck exploration, BNE: bilateral neck exploration.
Source: Data from [23].
283
PARATHYROID
Table 20.5. Prospective, quasi-experimental studies of unilateral neck exploration
Study
Author
population
Russell [24] 90 PHPT
Norman
[17]
18 PHPT with a
single
adenoma
Wei [21] 33 sporadic
PHPT with a
solitary
adenoma
Carty [26] 128 sporadic
PHPT
Moore [27] 48 sporadic
PHPT
PHPT: primary hyperparathyroidism, UNE: unilateral neck exploration, BNE: bilateral neck exploration, io-PTH: intraoperative PTH assay, US:
ultrasonography.
Note: Studies with minimally invasive (focused) surgery were excluded.
Preoperative
imaging Intervention Results
201
99m
Tl-
Tc scan Scan-directed UNE (n = 48)
Removal of adenoma and biopsy of
the ipsilateral normal gland
Conversion to BNE if necessary
BNE when the scan negative or UNE
failed (n = 42)
Identification of all four
parathyroids
Removal of obviously enlarged
UNE/BNE = 48/42
Cure rate 100% in the UNE
patients at mean
follow-up of 16.8 months
(n = 46)
Persistent hypercalcemia
14% who needed BNE
(6/42)
glands and biopsy of one normal-
99m
Tc sestamibi
scan
sized gland
UNE
Removal and frozen section of an
enlarged gland and search of a
UNE/BNE = 18/0
Cure rate: 100% (18/18) at 6
months after surgery
normal ipsilateral gland
99m
Tc sestamibi
scan
Conversion to BNE if necessary
UNE followed by contralateral
exploration
Removal of an enlarged gland and
Cure rate: 100% (33/33)
UNE would save
approximately 30 min
search and biopsy of a normal
ipsilateral gland
Additional exploration and biopsy
of contralateral glands
Limited to high-
risk patients in
Strategy A;
routine in
Strategy B.
Strategy A (n = 61)
Palpation method for selective UNE
Conversion to BNE if necessary
Strategy B (n = 67)
Routine use of both 99mTc
sestamibi SPECT and ioPTH
Removal of an enlarged gland and
search and biopsy of a normal
Strategy A
UNE/BNE = 25/36
Cure rate at 6 months: 95%
(58/61)
Strategy B
UNE/BNE = 42/25
Cure rate at 6 months: 99%
(66/67)
ipsilateral gland
99m
Tc sestamibi
scan, US if the
scan failed.
Conversion to BNE if necessary
UNE when the scan/US indicated a
single disease, or both failed
localization
Removal of adenoma and biopsy of
an ipsilateral normal gland
Use of io-PTH
Use of a handheld scintillation
UNE 32 (67%)
UNE >> BNE 13 (27%)
BNE 3 (6%)
Cure rate 98% (47/48) at 3
months after surgery
detector when an adenoma could
not be found on the predicted side
Conversion to BNE if necessary
BNE when the scan indicated bilateral
disease
284
ENDOCRINE SURGERY
et al. compared two surgical approaches to
concise parathyroidectomy. Routine use of preoperative
99m
Tc sestamibi single photon emission
computed tomography and intraoperative quick
PTH measurement was associated with significant
reductions in extent of surgery (i.e., more unilateral neck exploration) and the cure rate of 99%
unilateral neck exploration directed by preoperative localization techniques could be successful
in around 60–70% of patients with seemingly
sporadic primary hyperparathyroidism, and that
cure rate can achieve over 95% given the contralateral side be explored if necessary and/orwith the
use of intraoperative quick PTH measurement.
[26]. Moore and others examined the efficacy
of unilateral neck exploration with the aid of
preoperative localization modalities and intraoperative PTH measurements. Unilateral neck
Experimental Studies (Randomized
Controlled Trials)
exploration was planned when the preoperative
imaging studies indicated a single gland disease
although bilateral search was made as needed.
Thirty-two of the 48 patients (67%) had successful
unilateral exploration while 16 patients ultimately
underwent bilateral operation.Actualcurerateof
this approach was 98% at 3 months after surgery
[27]. These prospective studies suggested that
Table 20.6. Randomized controlled trial comparing unilateral (including focused parathyroidectomy) and bilateral neck
explorations for primary hyperparathyroidism
Study population Intervention Outcomes
Miccoli [28] 38 sporadic
PHPT suitable
for VAP (i.e.,
ultrasonography
indicates a
solitary
adenoma)
Bergenfelz [29]
Westerdahl
[30]
91 sporadic PHPT UNE group (n = 47):
VAP group (n = 20) :
Focused removal of an
adenoma
Use of io-PTH
Conversion to BNE if
necessary
BNE group (n = 18) :
Identify four glands
Removal and frozen section
of an enlarged gland
No biopsy of normal sized
gland
No io-PTH
Preoperative MIBI scan
Focused removal of an
adenoma
Use of io-PTH
Conversion to BNE if UNE
failed to make sure cure
BNE group (n = 44):
No localization studies
Identify four glands
Removal and frozen section
of an enlarged gland
No biopsy of normal sized
gland
No io-PTH
To date four randomized controlled trials com-
paring unilateral neck exploration with bilateral
approach have been published; yet, it should be
noted that the experiments differed in terms of
study populations, interventions, and outcome
measures [28–32]. (Table 20.6). In particular,
three of them utilized focused removal of an
Conversion to BNE in VAP group: 1/20 (5%)
Cure rate:
19/19 (100%) in VAP group
17/17 (100%) in BNE group
*1/20 (5%) in VAP group and 1/18 (6%) in BNE
group were excluded from the analysis because
they were found to have multi-glandular
disease
Conversion to BNE in the UNE group: 18/47 (38%)
Cure rate at 6 weeks after surgery:
45/47 (96%) in UNE group
43/44 (98%) in BNE group
Recurrence rate at 5 years after surgery:
2/38 (5%) in UNE group
1/33 (3%) in BNE group
Overall 6 patients have found to have persistent (3)
or recurrent (3) primary hyperparathyroidism.
Three of the 6 patients have found to have
multiple endocrine neoplasia mutations
285
PARATHYROID
Table 20.6. (continued)
Study population Intervention Outcomes
Bergenfelz [31] 50 PHPT with a
solitary
adenoma
localized by
99m
Tc sestamibi
scan.
Russell [32] 100 PHPT whose
single tumor
was identified
at operation at
the site
suggested by
the
preoperative
dual-isotope
subtraction
scanning using
99m
Tc and Tclabeled
sestamibi
PHPT: primary hyperparathyroidism,
VAP: video-assisted parathyroidectomy,
MIP: minimally invasive parathyroidectomy,
BNE: bilateral neck exploration,
UNE: unilateral neck exploration,
io-PTH: intraoperative quick PTH measurement.
MIP ( n = 25)
Targeted resection of
adenoma
Io-PTH
Frozen-section analysis
Local anesthesia
Conversion to BNE if
necessary
BNE (n = 25)
Identify all four parathyroid
glands
Excision of enlarged glands
Frozen-section analysis
No io-PTH
General anesthesia
Scan-directed UNE (n = 54)
Removal of adenoma and
identification of the
ipsilateral normal gland
No io-PTH
BNE (n = 46)
Identify the two
parathyroids on the
contra-lateral side
Removal of obviously
enlarged glands
No io-PTH
Conversion to BNE in the MIP group: 3/25 (12%)
Cure rate at 1 and 6 months
MIP: 24/25
BNE: 25/25
Cure rate at a mean of 23 months’ follow-up.
UNE: 54/54
BNE: 46/46
adenoma rather than total unilateral exploration.
Miccoli et al. compared video-assisted parathyroidectomy (VAP) against conventional bilateral
neck exploration (bilateral neck exploration) with
a study population consisting of 38 patients with
sporadic primary hyperparathyroidism suitable
for VAP (i.e., ultrasonography indicated a solitary
parathyroid adenoma). Cure rates were 100% in
both groups while the VAP group experienced
less costs, shorter operative times, less pain, and
better cosmetic results than the bilateral neck
exploration group [28]. Bergenfelz and others
allocated either unilateral neck exploration or
bilateral neck exploration to 91 patients with seemingly sporadic primary hyperparathyroidism.
Patients in the unilateral neck-exploration group
underwent both preoperative
99m
Tc sestamibi scan
and intraoperative monitoring of serum PTH
whereas those in the bilateral neck-exploration
group had neither localization studies nor intraoperative PTH measurement. In the unilateral
group, no attempts were made to visualize normal
286
ENDOCRINE SURGERY
parathyroid glands. Cure rates, operative time,
cost, and postoperative pain were similar between
the two groups [29]. Results of 5-year follow-up of
the trial have recently been reported by Westerdahl
and Bergenfelz. In addition to three persistent
cases, three patients experienced disease recurrence, two in the unilateral neck exploration
group, and one in the bilateral neck exploration
group on the intention-to-treat analysis despite
the fact that five of them actually underwent
bilateral neck exploration [30]. A trial in
Germany randomized 50 patients with primary
hyperparathyroidism with a solitary adenoma
demonstrated by sestamibi scintigraphy to
either MIP under local anesthesia or bilateral
neck exploration under general anesthesia.
Cure rates by the primary surgery were 96% in
the MIP group and 100% in the bilateral
exploration group, respectively [31]. Russell
et al. compared scan-directed unilateral neck
exploration with bilateral one. In this trial,
100 patients were randomized to one of the
interventions during the surgery if a single
adenoma was identified at the site suggested
by the preoperative scintigraphy. All patients
were cured in both groups [32]. Noninferiority,
or even advantages, of unilateral neck exploration or focused parathyroidectomy have been
demonstrated through these randomized controlled trials.
Bilateral Versus
Unilateral Neck Exploration:
In Practice
Evidence demonstrated that unilateral neck
exploration or focused surgery with adequate
preoperative imaging procedures and intraoperative quick PTH measurement have, on aver-
age, equivalent cure rate and even less invasive
when compared with the use of bilateral neck
exploration in treating primary hyperparathyroidism. On an individual basis, however, select-
ing a particular surgical approach depends
on various factors. In addition to the expertise
of surgeons and the validity of preoperative localization studies available, the success of the
limited approach is highly dependent on the
possibility of multiple gland disease of the individual [33].
Possibility of Multiglandular
Disease – Prevalence
The prevalence of multiglandular disease in primary hyperparathyroidism had been estimated
to be around 15% [29]. In 1996, Moliani et al.
found the figure to be 5% in their prospective
study where 110 patients with seemingly sporadic primary hyperparathyroidism underwent
focused parathyroidectomy using quick intraoperative PTH measurement [34]. Lee and Norton reviewed their 214 consecutive patients who
underwent bilateral neck exploration and found
that 44 (20.6%) had multiglandular disease,
although they did not indicate whether they
excluded patients with multiple endocrine neoplasia from the study population [35]. In the
same article, the authors conducted a literature
review to determine the prevalence of single
adenoma and multiglandular disease in published studies of unilateral and bilateral neck
exploration for primary hyperparathyroidism.
Retrieved articles were grouped according to
operative technique irrespective of study design
and study population. Of 2,166 patients in 14
studies who underwent bilateral neck exploration, 19.3% had multiglandular disease, whereas
the prevalence was found to be 5.3% among
2,095 patients from 31 published reports adopting a focused unilateral approach [35]. As the
authors cited, the observed difference in the
prevalence can be explained in some ways.
First, selection bias may play a role in assembling study populations. Patients whose preoperative localization studies indicated multiglandular disease were less likely to be
candidates for unilateral or even focused operations. Second, the definition of multiglandular
disease could be different among selected studies, namely functional versus morphological
[29]. Thus studies with unilateral exploration
might underestimate the prevalence while
those with bilateral approach might overestimate the figure. Prevalence data of multiglandular disease from four prospective studies and four randomized trials cited in the
previous sections were summarized in
Table 20.7. Although exact histopathological
diagnoses of multiglandular disease were not
described in three randomized trials, the
overall prevalence ranged from 0 to 15%. It
should be noted that the confidence intervals
287
PARATHYROID
Table 20.7. Prevalence of multiglandular disease observed in prospective studies
Definition of multiple gland
Author Study design
Russel [24] Prospective, quasi-
experimental
Wei [21] Prospective, quasi-
experimental
Carty [26] Prospective, quasi-
experimental
Moore [27] Prospective, quasi-
experimental
Miccoli [28] Randomized controlled
trial
Bergenfelz [29]
Westerdahl [30]
Bergenfelz [31] Randomized controlled
Russell [32] Randomized controlled
VAP: video-assisted parathyroidectomy, MIP: minimally invasive parathyroidectomy, BNE: bilateral neck exploration, UNE: unilateral neck
exploration, io-PTH: intraoperative quick PTH measurement.
Randomized controlled
trial
trial
trial
disease
Not described Hyperplasia 7% (3/42 underwent
Not described 0% (0/33 underwent BNE)
Not described. Hyperplasia 9% (11/128)
Not described. Hyperplasia 2% (1/48)
Morphological (BNE) and
functional (VAP)
UNE group: functional and
histopathology
BNE group: histopathology
MIP group: functional and
histopathology
BNE group: histopathology
Histological 0% (0/54) in UNE group
Prevalence of multiple gland
disease
BNE)
Double adenomas 4% (5/128)
Double adenomas 13% (6/48)
5% (1/20) in VAP group
6% (1/18) in BNE group
Overall 5% (2/38).
13% (6/47) in UNE group
11% (5/44) in BNE group
Overall 12% (11/91)
4% (1/25) in MIP group
8% (2/25) in BNE group
Overall 6% (3/50).
7% (3/46) in BNE group (Double
adenomas)
Overall 3% (3/100)
of the figures should be fairly large because
the numbers of patients in each study were
relatively small.
Possibility of Multiglandular
Disease – Clinical Characteristics
One of the important clinicians’ jobs is to characterize a patient so that tests and interventions
can fit her or his best outcomes. In fact, the
ultimate goal of clinical epidemiology is to contribute this through thoughtful use of available
evidence. Kebebew et al. developed a scoring
model with data of preoperative clinical, biochemical, and imaging studies to differentiate
patients with single from multiple gland disease
by reviewing medical record of 238 consecutive
patients with primary hyperparathyroidism
including multiple endocrine neoplasia as
well as persistent or recurrent diseases [36].
Their CaPTHUS dichotomous scoring model
consisted of five variables: (1) preoperative
total calcium level 3 mmol/l (12 mg/dl); (2)
intact PTH level 2 times the upper limit of
normal PTH levels; (3) sestamibi scan results
positive for one enlarged parathyroid gland;
(4) neck ultrasound results positive for one
enlarged parathyroid gland; and (5) concordant
sestamibi and neck ultrasound study results
(identifying one enlarged gland on the same
side of the neck). A total score of 3 or greater
had a sensitivity of 44% and specificity of 100%
in predicting single-gland disease. Since there
were no false positives, the authors concluded
that patients with a score of 3 or higher could
undergo an MIP without the routine use of
intraoperative PTH or additional imaging
studies. The model, however, remains to be
validated because it was derived from a retrospective analysis. In fact, even before developing the model, the authors were successful in
curing 99.2% of their patients in which 65%
underwent unilateral or focused neck
288
ENDOCRINE SURGERY
Table 20.8. Conditions when bilateral neck exploration needs to be considered
Family history
p
p
p
Biochemical data
Localization studies
p
p
p
p
p
p
Intraoperative findings at UNE
UNE: unilateral neck exploration.
p
p
explorations. Although such a quantitative
model can be useful, it may be more practical
to consider each characteristic associated with
multiglandular disease in individualizing the
decision as to whether the neck should be
explored bilaterally or not (Table 20.8).
Conclusions
There is no doubt that bilateral neck exploration has been the gold standard as the surgical
procedure for primary hyperparathyroidism
[37]. With the advent of modern medical technologies, however, limited or focused
approaches have become suitable alternatives
for selected patients as the history has witnessed. An endocrine surgeon should use her
or his expertise with deep understandings of
the disease so that best outcomes are available
for each patient.
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