Download Protection of parathyroid glands in thyroid surgery and treatment of

Protection of parathyroid glands in thyroid
surgery and treatment of postoperative
hypocalcemia
Xue-hai BIAN, Hui SUN
Department of Thyroid Surgery, China–Japan Union
Hospital of Jilin University, Jilin Provincial Key Laboratory
of Surgical Translational Medicine
Changchun, China
E-mail: [email protected]
Background: Hypoparathyroidism is one of the most
frequent and serious complications of the thyroid surgery.
Preservation of parathyroid glands (PGs) and treatment of
postoperative hypocalcemia are key factors. The aim of this review is
to evaluate the relevant literature and provide the clinician guidance
for preservation of PGs and the formulation of individualized
therapeutic strategies for patients with postoperative hypocalcemia.
Methods: This was a review of preservation of PGs in
thyroidectomy procedures and treatment strategies for postoperative
hypocalcemia. Results: In-depth knowledge of the anatomy of
PGs along with relations and an adequate preoperative assessment are
the cornerstone for surgeons performing safe thyroid parathyroid
surgeries. The “capsular dissection” of the thyroid lobe is the key
technique to protect PGs and their supply blood vessels; the
intraoperative parathyroid autotransplantation if the occasion should
arise is an effective method to prevent definitive hypoparathyroidism.
The patients after thyroidectomy are given monitoring of the serum
calcium and parathyroid hormone (PTH); the early combinational
supplement treatment of calcium and calcitriol effectively prevent
postoperative hypocalcemia. Conclusion: To master the anatomic
regularity of PGs, intraoperative in-situ conservation and
autotransplantation of PGs, and postoperative individualized
therapeutic strategies of hypoparathyroidism are effective methods to
avoid hypocalcemia in thyroid surgery.
Key
words Parathyroid;
Hypoparathyroidism; Thyroidectomy
Thyroid;
Hypocalcemia;
INTRODUCTION
Hypoparathyroidism is one of the most frequent and
serious complications of the thyroid surgery. Preservation of
PGs and treatment of postoperative hypocalcemia are key
factors. Incidence of postoperative hypoparathyroidism is
reported from 1.7-68%[1-3]. Clinically, patients characterized
by hypocalcemia which usually mild, but sometimes is severe.
As for duration, hypocalcemia can be transitory, shorter than 6
months (most often), or permanent – longer than 6 months[1, 4].
Hypocalcemia can lead to significant morbidity and impaired
quality of life. This complication of thyroidectomy has been
attributed to not only the extent of disease, previous thyroid
operations, and other factors, but also more important, without
thorough understanding of PGs anatomy [5], the troubled
operative technique from inexperienced hands during surgical
maneuvers [4], and improper disposal to postoperative
hypocalcemia[6]. The latter is improved by training and
enhancing the operative technology. This article reviews the
current literature on technologies for protecting PGs,
individualized therapeutic strategies of hypoparathyroidism
and is focusing on reducing postoperative hypocalcemia in
thyroid surgery.
IDENTIFICATION
OF
PGS
Technological assessment of CT, MRI and PET-CT
Computed tomography (CT) and magnetic resonance
imaging (MRI) are advanced imaging modalities that are not
typically utilized as part of the initial evaluation of thyroid and
parathyroid pathology. However, both modalities have
applications in complex cases, particularly in the reoperative
setting and in operative planning for initial or recurrent
carcinomas. As part of a multimodal approach, CT and MRI
can increase the successful preoperative localization of
abnormal parathyroid glands. Newer imaging modalities, such
as PET-CT and SPECT-CT in thyroid imaging, and 4D-CT in
parathyroid imaging, can provide information on the anatomy
as well as the function of pathologic tissues. Both modalities
provide excellent assessment of the extent of disease, local
invasion and distant metastases[7]. The combined functional
and anatomical modality of choline PET/CT is a promising
tool for parathyroid adenoma localization, providing clearer
images than MIBI, equal or better accuracy, and quicker and
easier acquisition[8, 9].
Visual representation identification
Presently, the endoscopic thyroidectomy and the robotic
thyroidectomy can reduce scarring and postoperative neck
discomfort has been universally accepted by both the patient
and the surgeon[10-12]. One of the advantages of two
technologies over open surgery offers improved magnified
visual representation. Some present studies demonstrated
robotic thyroidectomy for thyroid cancer patients had
perioperative better outcomes and shorter learning curve, as
3D magnified stereoscopic surgical view and flexible
instrumentation[12-14]. There were no significant differences
between the two technologies and conventional open surgery
at the incidence of postoperative permanent and transient
hypocalcemia[15, 16]. Despite these benefits, the
identification of PGs on visual representation lacks the sense
of touch, so still relies on the mastery of anatomy of PGs.
Thus, large prospective randomized trials with longer-term
periods are needed to determine whether the endoscopic
thyroidectomy and the robotic thyroidectomy are beneficial in
the identification of PGs and impact the incidence of
postoperative hypocalcemia.
Advance
Recently, the carbon nanoparticle (CN) suspension
negative imaging has applied to identifying and protecting the
PGs during thyroid surgery. Nanocarbon granules have 150nm
diameters which enter lymphatic capillaries with 500nm
diameters, but not blood vessel capillaries with 30-50nm. The
thyroid has rich lymphatic capillaries in, whereas there are
almost none within the PGs[17, 18]. CN suspension being
injected to thyroid tissues immediately enter into the thyroid
capillary lymphatics, stain the thyroid gland and the
surrounding lymph nodes black but not the PGs, which could
easily distinguish the anatomical boundaries among lymphoid
tissue, thyroid tissue, and PGs[18], especially in central
cervical lymph node dissection. Huang et al.[18] recent study
suggested that CN suspension injections in thyroid cancer
surgery assisted identification of the PGs was significant to
decrease the incidence of symptomatic postoperative
hypocalcemia. Although the efficacy of this new technique is
still controversial [19], the further researches have being
performed by multicenter in China.
Some authors [20, 21] reported the rapid intraoperative
parathyroid hormone (rIO-PTH) assay in fine needle
aspiration was used for differential diagnosis in thyroid
surgery. Direct aspiration of the suspected parathyroid tissue
，then the rIO-PTH was analyzed within 15 min of receiving
the sample. Bian et al. [22]reported the rIO-PTH values
obtained on the PGs range from 145.2 pmol/L to 5,000
pmol/L, with a rIO-PTH median of 3,369 pmol/L, and
indicated it was a simple, low-cost and non-invasive technique
to distinguish between the PGs and the lymph nodes that can
be performed in real time. However, presently, rIO-PTH
values tissue aspirates still are correlated with pathological
diagnosis, rIO-PTH values has no standard. Whether this
technique can replace frozen-section examination is need to
research from a large number of cases.
Many experimental techniques have been tried for
recognizing parathyroid tissue. Fluorescence diagnosis using
aminolevulinic acid, a photodynamic reagent is an endogenous
precursor in the biosynthesis of human hemoglobulin, has
been described to identify normal PGs in rats, which showed
red fluorescence of PGs was observed by surrounding tissue
under direct vision[23, 24]. Prosst et al. [25] used this
technique for intraoperative localization of PGs in patients
with primary and secondary hyperparathyroidism, who were
performed minimally invasive parathyroidectomy with
fluorescence-guided. Some authors reported the methylene
blue via a 200–500ml fluid infusion volume before skin
incision was available to aid localization of enlarged PGs
during surgery for hyperparathyroidism[26, 27]. King, et al.
[28] used the antiparathyroid antibody BB5-G1 conjugated to
cibacron blue to stain human parathyroid implants in athymic
nude mice was intravenously infused to enhance parathyroid
visualization. Grubbs[29] indicated the gamma probe
identification was a simple and effective technique for
parathyroid preservation. The patients underwent preoperative
intravenous injection of 99mtechnetium-labeled sestamibi,
where after the intraoperative Neoprobe Control Unit was
used to identify relatively higher focal gamma activity to
localize PGs both in situ as well as ex vivo in the resected
specimen. The above new techniques could be of great benefit
to patients, however, most of them are in an experimental
stage and the clinical applications are limited ， the further
investigation should be considered.
IN-SITU
CONSERVATION OF
PGS
Identification of the PGs is the premise, and conservation
of PGs and their supply blood vessels is the key technique to
prevent PGs’ function impairment and postoperative
hypocalcemia[30]. The practice in our hospital is that,
preservation of the PGs in situ is instead of performing
autotransplantation unless an accidental removal and poor
blood supply(Fig.1).
Thompson[31] recommended the “capsular dissection”
techniques of the thyroid lobe, dissection along the plane
between the true and false capsules of the thyroid, and ligating
and dividing the branch of vessels close to the true capsule, in
order to preserve each PG and its blood supply in under direct
vision. The false thyroid capsule plays an important role in
capsular dissection[32]. A deep understanding of anatomy of
the true and the false capsule of thyroid glands is beneficial to
identifying the correct dissection plane[33].
Surgeons who perform thyroidectomy are suggested to
start from the superior pole of the thyroid lobe, divide and
ligate the middle thyroid vein. Medially rotation of the lobe to
the trachea central surface provides exposure to posterolateral
surface of thyroid lobe. Hemostatic clamps are applied
carefully to the capsule of the thyroid lobe along its lateral
edge. The dissections using bipolar diathermy or Harmonic
scalpel proceed along the plane between the true and false
capsules of the thyroid, not to dissect in a subcapsular plane
which leads to increased bleeding, meanwhile, the false
thyroid capsule carefully is pulled inferolaterally for
identification of the PGs and the RLN. As the initial step, the
focus of the dissection should be to identify and preserve the
PGs along with their vascular supply instead of identifying the
RLN laterally in the paratracheal groove. Dissection should
stay close to the true capsule, otherwise, the possible injury
that may occur to PGs along with their blood supply[33]. It is
essential that the terminal branches of the superior and inferior
thyroid arteries are ligated close to the thyroid capsule using
the fine-tipped bipolar diathermy or Harmonic scalpel. The
aim is that these vessels are ligated distal to PGs, so that their
division will allow the PGs to be reflected off the thyroid,
without compromise of their blood supplies[34]. Finally, the
entire thyroid lobe was dissected out by dividing the Berry’s
ligament.
Surgeons
who
perform
thyroidectomy
must
intraoperatively pay more attention to the followings: 1. To
master the indication of the total thyroidectomy strictly, select
operative methods correctly, the total thyroidectomy should
not be performed blindly. 2. To operate gently, the operative
field should be kept dry and clear. 3. Don't clamp the posterior
thyroid capsule blindly. 4. To reduce the power of diathermy
to prevent thermal damage and form tiny blood clots in the
distal branches of thyroid arteries. 5. To keep their distance
from Harmonic scalpel to the posterior thyroid capsule to
avoid thermal damage. 6. To keep observation of PGs color
changes. If the vascular supply is damaged, the color of PGs
will be changed gradually from yellowish brown to dim to
atropurpureus for ischemia. Some PGs may lead to a certain
degree of ischemia due to thrombosis, although their vascular
supply is preserved completely, in those cases may recover
after 10-30 min generally. If congestion is found under
parathyroid capsule, we acupuncture the capsule using a
needle to release the hematoma blood to prevent atrophy
degeneration. 7. Occasionally, PGs are encountered densely
adherent to the thyroid capsule by multiple small blood
vessels, especially thyroiditis. In cases of PGs becoming
detached from their blood supply and/or becoming majorly
discolored, the glands are removed and autotransplanted.
AUTOTRANSPLANTATION OF PGS
The application of PGs autotransplantation during thyroid
surgery
is
an
effective
method
to
prevent
definitive hypoparathyroidism and
to
decrease
the
postoperative incidence of transient hypocalcaemia[35], also is
a physiological breakthrough in the field of thyroid
surgery[36]. Intraoperatively, if an inadvertently removal PGs
is found in the removed specimen, then it definitely should be
transplanted[36, 37]. On the other hand, PGs
autotransplantation should be performed for avulsed or
devascularized PGs[38] or if the blood supply appears to be
compromised[36, 39, 40]. It is the key that the
autotransplanted PGs can survive for a long time and secrete
PTH. The PTH level resumes within 2-4 weeks after
autotranplantation[41, 42], parathyroid tissues become fully
functional at 2 months when biochemical functional
assessment
was
performed
after
forearm
PGs
autotranplantation[42].
Thus,
the
value
of
PGs
autotranplantation can be confirmed[43], there is no doubt that
this technique should be routinely and decidedly performed
for inadvertently removal or devascularised PGs during
thyroidectomy.
Before the autotranplantation of PGs, routine frozen
section examination of parathyroid biopsy has been performed
to confirm parathyroid tissue and avoid reimplantation of
potentially malignant tissue[37-39, 44]. A mimimal amount of
parathyroid tissue can confirm pathologically, and a maximal
amount of parathyroid tissue is saved. On the other hand, the
practice in our hospital is that, when the intraoperative blood
PTH levels are inferior to 15 pg/ml or reduced over 75%
compared with preoperative PTH levels 30 min after excision,
a searching for an inadvertently PGs conscientiously is
performed in the removal biopsy, especially the biopsy from
the central cervical lymph node dissection for thyroid
carcinoma patients(Fig.1).
The inadvertently removal or devascularised PG is placed
in saline at 4℃ as soon as possible after excision. After
cooling for 30 min, the PG is sufficiently firm to be minced
into 1×1mm. Generally, pieces are inserted into the ipsilateral
sternocleidomastoid muscle. The PGs auto-transplanted into
sternocleidomastoid muscle is convenient and effective during
thyroidectomy[41]. The brachioradialis muscle in the forearm
is usually employed as the implantation site for abnormal or
hyperplastic parathyroid tissue during parathyroid surgery[37,
45].
TREATMENT
OF POSTOPERATIVE
HYPOPARATHYROIDISM
Some authors[46] reported the frequency of transient
hypoparathyroidism (which resolved until 6 months) and
permanent, after total thyroidectomy, was 5.2% and 1.1%,
respectively. Postoperative transient hypoparathyroidism may
be caused by temporary poor blood supply of PGs, whereas
permanent hypoparathyroidism may be due to ischemic
necrosis of PGs or inadvertently removal. The principle
treatment of hypocalcemia according to most of the
informations published: the symptomatic treatment is
performed in the patients with the transient hypocalcemia; try
to enhance in serum calcium, decrease the unpleasant
symptoms and the complications of the permanent
hypocalcemia.
Toniato et al. have demonstrated the efficacy of sampling
blood iPTH levels 30 min after the end of the operation,
establishing the indication of calcium supplement when the
blood levels were inferior to 15pg/ml[47]. Cmilansky et al.
reported the sensitivity of iPTH<15pg/ml in predicting the
development of hypocalcemia was 71% and specificity, 99%.
The positive predicting value was 97% and negative
predicting value was 86%[4]. We prefer to prophylactically
give a calcium supplement, either intravenously or orally, to
all patients at high risk of hypocalcemia whose iPTH levels
after the end of the operation are inferior to 15pg/ml or drop
over 75% lower. Patients after thyroidectomy who show both
serum calcium under 8.0 mg/dL and any symptoms of
hypocalcemia, including any paresthesia, numbness, or muscle
cramps require calcium or vitamin D supplement treatment
and monitoring of the serum calcium(Fig.1).
Only symptomatic patients with serum calcium >2mmol/L
are supplemented with oral calcium 0.5–1.5g/day. Those with
serum calcium 1.8–2mmol/L obtain oral calcium 1–2g/day,
while in cases of serum calcium <1.8mmol/L and with severe
symptoms calcium is administered intravenously and orally,
meanwhile is given oral calcitriol 0.5–1.0μg/day. The cases
suffer from hypocalcemia crisis are supplemented with
intravenous injection calcium gluconate 2g immediately. The
patients may relieve symptoms and control muscle spasms
quickly, then calcium gluconate 3g is administered
intravenous drip (8 -10 h). Although Cmilansky et al. [4]
recommended that calcitriol was administered in ca ses with
low serum calcium and iPTH only after endocrinology
consultation. Roh et al. [48] results showed that the early
combinational supplementation of calcium and calcitriol more
effectively prevented postoperative hypocalcemia than
calcium alone. To prevent the parathyroid vessel vasospasm
and thrombosis, vasodilators should appropriately be
recommended to protect the blood supply and ensure
parathyroid function postoperatively (Fig.1).
[9]
[10]
[11]
[12]
[13]
[14]
[15]
[16]
[17]
Acknowledgment
Natural Science Foundation of Jilin Provincial Science and
Technology Department (No.3D512Z843430-1).
References
[1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
T. Reeve and N. W. Thompson, "Complications of thyroid surgery: how
to avoid them, how to manage them, and observations on their possible
effect on the whole patient," World J Surg, vol. 24, pp. 971-5, Aug 2000.
R. M. Quiros, C. E. Pesce, S. M. Wilhelm, G. Djuricin, and R. A. Prinz,
"Intraoperative parathyroid hormone levels in thyroid surgery are
predictive of postoperative hypoparathyroidism and need for vitamin D
supplementation," Am J Surg, vol. 189, pp. 306-9, Mar 2005.
L. Rosato, N. Avenia, P. Bernante, M. De Palma, G. Gulino, P. G. Nasi,
et al., "Complications of thyroid surgery: analysis of a multicentric study
on 14,934 patients operated on in Italy over 5 years," World J Surg, vol.
28, pp. 271-6, Mar 2004.
P. Cmilansky and L. Mrozova, "Hypocalcemia - the most common
complication after total thyroidectomy," Bratisl Lek Listy, vol. 115, pp.
175-8, 2014.
R. D. Bliss, P. G. Gauger, and L. W. Delbridge, "Surgeon's approach to
the thyroid gland: surgical anatomy and the importance of technique,"
World J Surg, vol. 24, pp. 891-7, Aug 2000.
A. G. Pfleiderer, N. Ahmad, M. R. Draper, K. Vrotsou, and W. K.
Smith, "The timing of calcium measurements in helping to predict
temporary and permanent hypocalcaemia in patients having completion
and total thyroidectomies," Ann R Coll Surg Engl, vol. 91, pp. 140-6,
Mar 2009.
R. Warren Frunzac and M. Richards, "Computed Tomography and
Magnetic Resonance Imaging of the Thyroid and Parathyroid Glands,"
Front Horm Res, vol. 45, pp. 16-23, 2016.
M. Orevi, N. Freedman, E. Mishani, M. Bocher, O. Jacobson, and Y.
Krausz, "Localization of parathyroid adenoma by (1)(1)C-choline
PET/CT: preliminary results," Clin Nucl Med, vol. 39, pp. 1033-8, Dec
2014.
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
[26]
[27]
M. Gahier Penhoat, D. Drui, C. Ansquer, E. Mirallie, Y. Maugars, and P.
Guillot, "Contribution of 18-FDG PET/CT to brown tumor detection in a
patient with primary hyperparathyroidism," Joint Bone Spine, Oct 07
2016.
Y. S. Chung, J. H. Choe, K. H. Kang, S. W. Kim, K. W. Chung, K. S.
Park, et al., "Endoscopic thyroidectomy for thyroid malignancies:
comparison with conventional open thyroidectomy," World J Surg, vol.
31, pp. 2302-6; discussion 2307-8, Dec 2007.
Y. L. Park, W. K. Han, and W. G. Bae, "100 cases of endoscopic
thyroidectomy: breast approach," Surg Laparosc Endosc Percutan Tech,
vol. 13, pp. 20-5, Feb 2003.
J. Lee and W. Y. Chung, "Robotic surgery for thyroid disease," Eur
Thyroid J, vol. 2, pp. 93-101, Jun 2013.
N. D. Perrier, G. W. Randolph, W. B. Inabnet, B. F. Marple, J.
VanHeerden, and R. B. Kuppersmith, "Robotic thyroidectomy: a
framework for new technology assessment and safe implementation,"
Thyroid, vol. 20, pp. 1327-32, Dec 2010.
R. B. Kuppersmith and F. C. Holsinger, "Robotic thyroid surgery: an
initial experience with North American patients," Laryngoscope, vol.
121, pp. 521-6, Mar 2011.
J. J. Jeong, S. W. Kang, J. S. Yun, T. Y. Sung, S. C. Lee, Y. S. Lee, et
al., "Comparative study of endoscopic thyroidectomy versus
conventional open thyroidectomy in papillary thyroid microcarcinoma
(PTMC) patients," J Surg Oncol, vol. 100, pp. 477-80, Nov 1 2009.
W. W. Kim, J. S. Kim, S. M. Hur, S. H. Kim, S. K. Lee, J. H. Choi, et
al., "Is robotic surgery superior to endoscopic and open surgeries in
thyroid cancer?," World J Surg, vol. 35, pp. 779-84, Apr 2011.
S. W. Gray, J. E. Skandalakis, and J. T. Akin, Jr., "Embryological
considerations of thyroid surgery: developmental anatomy of the
thyroid, parathyroids and the recurrent laryngeal nerve," Am Surg, vol.
42, pp. 621-8, Sep 1976.
K. Huang, D. Luo, M. Huang, M. Long, X. Peng, and H. Li, "Protection
of parathyroid function using carbon nanoparticles during thyroid
surgery," Otolaryngol Head Neck Surg, vol. 149, pp. 845-50, Dec 2013.
Z. Zhang and Y. Wang, "Is carbon nanoparticle useful in thyroid surgery
regardless of surgery extent and experience?," Otolaryngol Head Neck
Surg, vol. 150, p. 503, Mar 2014.
M. R. Pelizzo, A. Losi, I. M. Boschin, A. Toniato, G. Pennelli, N.
Sorgato, et al., "Rapid intraoperative parathyroid hormone assay in fine
needle aspiration for differential diagnosis in thyroid and parathyroid
surgery," Clin Chem Lab Med, vol. 48, pp. 1313-7, Sep 2010.
J. Horanyi, L. Duffek, R. Szlavik, I. Takacs, M. Toth, and L. Romics,
Jr., "Intraoperative determination of PTH concentrations in fine needle
tissue aspirates to identify parathyroid tissue during parathyroidectomy,"
World J Surg, vol. 34, pp. 538-43, Mar 2010.
X. H. Bian, S. J. Li, L. Zhou, C. H. Zhang, G. Zhang, Y. T. Fu, et al.,
"Applicability of rapid intraoperative parathyroid hormone assay
through fine needle aspiration to identify parathyroid tissue in thyroid
surgery," Exp Ther Med, vol. 12, pp. 4072-4076, Dec 2016.
J. Gahlen, S. Winkler, C. Flechtenmacher, R. L. Prosst, and C. Herfarth,
"Intraoperative fluorescence visualization of the parathyroid gland in
rats," Endocrinology, vol. 142, pp. 5031-4, Nov 2001.
W. W. Liu, C. Q. Li, Z. M. Guo, H. Li, Q. Zhang, and A. K. Yang,
"Fluorescence identification of parathyroid glands by aminolevulinic
acid hydrochloride in rats," Photomed Laser Surg, vol. 29, pp. 635-8,
Sep 2011.
R. L. Prosst, J. Weiss, L. Hupp, F. Willeke, and S. Post, "Fluorescenceguided minimally invasive parathyroidectomy: clinical experience with a
novel intraoperative detection technique for parathyroid glands," World
J Surg, vol. 34, pp. 2217-22, Sep 2010.
D. B. Kuriloff and K. V. Sanborn, "Rapid intraoperative localization of
parathyroid glands utilizing methylene blue infusion," Otolaryngol Head
Neck Surg, vol. 131, pp. 616-22, Nov 2004.
H. P. Patel, D. R. Chadwick, B. J. Harrison, and S. P. Balasubramanian,
"Systematic review of intravenous methylene blue in parathyroid
surgery," Br J Surg, vol. 99, pp. 1345-51, Oct 2012.
[28] R. C. King, S. L. Mills, and J. E. Medina, "Enhanced visualization of
parathyroid tissue by infusion of a visible dye conjugated to an
antiparathyroid antibody," Head Neck, vol. 21, pp. 111-5, Mar 1999.
[29] E. G. Grubbs, E. A. Mittendorf, N. D. Perrier, and J. E. Lee, "Gamma
probe identification of normal parathyroid glands during central neck
surgery can facilitate parathyroid preservation," Am J Surg, vol. 196, pp.
931-5; discussion 935-6, Dec 2008.
[30] A. R. Shaha, "Revision thyroid surgery - technical considerations,"
Otolaryngol Clin North Am, vol. 41, pp. 1169-83, x, Dec 2008.
[31] N. W. Thompson, W. R. Olsen, and G. L. Hoffman, "The continuing
development of the technique of thyroidectomy," Surgery, vol. 73, pp.
913-27, Jun 1973.
[32] "Color atlas of thyroid surgery. Open, endoscopic and robotic
procedures," Anticancer Res, vol. 34, p. 3236, Jun 2014.
[33] Y. H. Tan, G. N. Du, Y. G. Xiao, S. Q. Guo, T. Wu, P. Z. Chen, et al.,
"The false thyroid capsule: new findings," J Laryngol Otol, vol. 127, pp.
897-901, Sep 2013.
[34] . A. Prinz, H. L. Rossi, and A. W. Kim, "Difficult problems in thyroid
surgery," Curr Probl Surg, vol. 39, pp. 5-91, Jan 2002.
[35] M. Testini, A. Gurrado, G. Lissidini, and M. Nacchiero,
"Hypoparathyroidism after total thyroidectomy," Minerva Chir, vol. 62,
pp. 409-15, Oct 2007.
[36] A. D. Katz, "Parathyroid autotransplantation in patients with parathyroid
disease and total thyroidectomy. Indications in 117 cases," Am J Surg,
vol. 142, pp. 490-3, Oct 1981.
[37] D. S. Baumann and S. A. Wells, Jr., "Parathyroid autotransplantation,"
Surgery, vol. 113, pp. 130-3, Feb 1993.
[38] A. R. Shaha, C. Burnett, and B. M. Jaffe, "Parathyroid
autotransplantation during thyroid surgery," J Surg Oncol, vol. 46, pp.
21-4, Jan 1991.
[39] J. A. Olson, Jr., M. K. DeBenedetti, D. S. Baumann, and S. A. Wells, Jr.,
"Parathyroid autotransplantation during thyroidectomy. Results of long-
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48]
term follow-up," Ann Surg, vol. 223, pp. 472-8; discussion 478-80, May
1996.
C. Y. Lo and K. Y. Lam, "Postoperative hypocalcemia in patients who
did or did not undergo parathyroid autotransplantation during
thyroidectomy: a comparative study," Surgery, vol. 124, pp. 1081-6;
discussion 1086-7, Dec 1998.
H. Funahashi, Y. Satoh, T. Imai, M. Ohno, T. Narita, M. Katoh, et al.,
"Our technique of parathyroid autotransplantation in operation for
papillary thyroid carcinoma," Surgery, vol. 114, pp. 92-6, Jul 1993.
C. Y. Lo and S. C. Tam, "Parathyroid autotransplantation during
thyroidectomy: documentation of graft function," Arch Surg, vol. 136,
pp. 1381-5, Dec 2001.
C. Y. Lo, "Parathyroid autotransplantation during thyroidectomy," ANZ
J Surg, vol. 72, pp. 902-7, Dec 2002.
R. P. Walker, E. Paloyan, T. F. Kelley, C. Gopalsami, and H. Jarosz,
"Parathyroid autotransplantation in patients undergoing a total
thyroidectomy: a review of 261 patients," Otolaryngol Head Neck Surg,
vol. 111, pp. 258-64, Sep 1994.
S. A. Wells, Jr., A. J. Ross, 3rd, J. K. Dale, and R. S. Gray,
"Transplantation of the parathyroid glands: current status," Surg Clin
North Am, vol. 59, pp. 167-77, Feb 1979.
A. Shaha and B. M. Jaffe, "Complications of thyroid surgery performed
by residents," Surgery, vol. 104, pp. 1109-14, Dec 1988.
A. Toniato, I. M. Boschin, A. Piotto, M. Pelizzo, and P. Sartori,
"Thyroidectomy and parathyroid hormone: tracing hypocalcemia-prone
patients," Am J Surg, vol. 196, pp. 285-8, Aug 2008.
J. L. Roh, J. Y. Park, and C. I. Park, "Prevention of postoperative
hypocalcemia with routine oral calcium and vitamin D supplements in
patients with differentiated papillary thyroid carcinoma undergoing total
thyroidectomy plus central neck dissection," Cancer, vol. 115, pp. 2518, Jan 15 2009.