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Japanese Journal of
Clinical Oncology
Japanese Journal of Clinical Oncology, 2016, 46(7) 635–641
doi: 10.1093/jjco/hyw055
Advance Access Publication Date: 9 May 2016
Original Article
Original Article
Minimally invasive video-assisted lateral
neck lymphadenectomy for the papillary
thyroid carcinoma with cervical lymph
nodes metastasis
Bo Li1, Wenxing Zhao2, Lina Xu1, Jingfu Sun1, Bo Chen3, Guanying Yu4,
Lan Ye5, Maosong Gong1, Wei Cong1, and Yuzhong Qi1,*
1
Department of Thyroid Surgery, The Second Hospital of Shandong University, Shandong, People’s Republic of
China, 2Department of Operating Theatre, Jinan Central Hospital, Shandong, 3Department of Thyroid Surgery, Qilu
Hospital of Shandong University, Shandong, 4Department of Gastrointestinal Surgery, Jinan Central
Hospital, Shandong, and 5Department of Cancer Center, The Second Hospital of Shandong University, Shandong
*For reprints and all correspondence: Yuzhong Qi, Department of Thyroid Surgery, The Second Hospital of Shandong
University, 247 Bei Yuan Road, Jinan, Shandong, 250033, People’s Republic of China. E-mail: [email protected]
Received 22 February 2016; Accepted 31 March 2016
Abstract
Objective: Minimally invasive video-assisted technique has been successfully used in thyroidectomy to treat low- and intermediate-risk papillary thyroid cancer. But there was very little experience of this technique to be used in the lateral neck lymphadenectomy to treat papillary thyroid
cancer with lateral neck lymph node metastasis. This study aimed to verify the potential benefits
of a new minimally invasive video-assisted lateral neck lymphadenectomy that evaluated the likelihood of the surgical method as an alternative for thyroid carcinoma with lateral lymph node
metastasis.
Method: A total of 58 patients were retrospectively compared, which included two groups:
Following thyroidectomy and the central neck node dissection (level VI), the first group underwent
the conventional lateral neck lymphadenectomy and the other group underwent video-assisted
lateral neck lymphadenectomy. In addition to the comparison of treatment outcomes between the
new treatment and the conventional one, other parameters including operative time, length of
incision, operative hemorrhage, postoperative drainage, length and costs of hospitalization were
also compared.
Results: Patients who received the new surgical method had significantly shorter incisional length,
lower incidence of local skin paresthesia and shorter length of hospitalization when compared to
the conventional treatment.
Conclusions: Compared with the conventional lateral neck lymphadenectomy for cN1b-stage
papillary thyroid carcinoma, the new minimally invasive video-assisted lateral neck lymphadenectomy is a feasible and safe alternative for treatment of thyroid carcinoma with cervical lymph node
metastases since it has the advantages of less postoperative complications and better cosmetic
outcome.
Key words: papillary thyroid carcinoma, lateral neck lymphadenectomy, cervical lymph nodes metastasis, minimally invasive
video-assisted technology
© The Author 2016. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
635
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A minimally invasive surgery for thyroid carcinoma
Introduction
In the past 20 years, the average annual growth rate of thyroid cancer was 6.2%, which ranks the first in the incidence growth rate
among all solid tumors, and papillary thyroid cancer accounts for
almost 90% of overall thyroid malignancies (1). Thyroid surgery
plays a critical role in the treatment of thyroid cancer, which directly
increases the survival of the patients with thyroid malignancies
(2,3). Since the 19th century, conventional thyroid surgery has been
widely used for the treatment of malignant thyroid disease and has
significantly decreased the fatality rate (4). However, it was unsatisfactory due to its postoperative complications, such as the conspicuous scar, paresthesia, dysphagia and voice change (5,6). With the
progress in surgical techniques, surgeons began to pursue smaller
incisions for cosmetic purpose and better postoperative recovery by
reducing the surgical injury.
Minimally invasive video-assisted thyroidectomy has been used
for treating malignant thyroid diseases since 2002 (7,8), which only
requires a cervical incision of <2.0 cm for laparoscope insertion (9).
With the application of a modified retractor, an ultrasonic scalpel
and a recurrent laryngeal nerve detector (RLN detector), minimally
invasive thyroidectomy has been improved in operative fields and
postoperative outcomes. This new technique has offered better cosmetic results and less postoperative pain than conventional thyroidectomy, with similar complication rates (10–12). It is currently
considered as an ideal minimally invasive technique for the surgery
of early-stage thyroid carcinoma (11).
Although minimally invasive video-assisted thyroidectomy has
been successfully used to treat early-stage thyroid carcinoma
(10,13–15), its value in lateral neck lymphadenectomy still remains
controversial due to the difficulties in exposing and dissecting lateral
neck lymph nodes. Robot-assisted endoscopic thyroidectomy with
modified radical neck dissection has been successfully adopted in
treating those patients with thyroid carcinoma with lateral neck
node metastases, but very high cost and special equipment were
required (16–20).
In this article, we retrospectively compared the results obtained
in patients with papillary thyroid cancer (TNM staging: cN1b) who
underwent video-assisted lateral neck lymphadenectomy (VALNL)
to those who underwent the conventional surgical method to testify
the feasibility, safety and efficacy of the new method. Several parameters including operative time, length of incision, operative hemorrhage, postoperative drainage, the number of lateral neck lymph
nodes resected, incidence of lymphatic leakage and local skin paresthesia, length and cost of hospitalization were investigated.
conventional lymphadenectomy (CL) group and the minimally
invasive VALNL group. After the operations, the tissues removed
from the thyroid gland and lymph nodes were detected by a pathological test. Preoperative assessments including local skin paresthesia, shoulder function, voice change, thyroid ultrasonic examination,
thyroid function tests and methoxyisobutylisonitrile scan were performed for all patients. The methods used to measure the local skin
paresthesia were the examinations of superficial sensation, which
included tactile sense, pain sense and temperature sense. If any of
the three above examinations showed the cervical skin in surgical
operation area was abnormal, the patient was recorded as a case
with local skin paresthesia.
Ethics, consent and permissions
This study was a retrospective study. For this type of study, formal
consent is not required. Informed consent was obtained from all
individual participants included in the study. All patients have
agreed that their data of diseases were used for scientific research
and publishment.
Surgical techniques
Under general anesthesia, patients were placed in the supine position. A soft pillow was placed under the shoulders for keeping the
neck extended slightly.
The procedure for the total thyroidectomy and central
neck lymphadenectomy (level VI)
At the beginning of the operation, an incision of 4–6 cm in
length was made for exposing the whole thyroid (Fig. 1B, line 1).
The inferior thyroid vessel, the thyroid middle vein and the upper
pole of thyroid gland were cut off using the ultrasonic scalpel. After
identifying the RLN and the parathyroid glands (especially the
superior gland), they were separated gently from the posterior surface of the thyroid gland. Total thyroidectomy and central lymph
node (level VI) were achieved.
The surgical procedure for CL group
After total thyroidectomy and central neck lymphadenectomy (level VI),
a 15- to 20-cm arc-shaped incision was made at the anterior of the
neck (Fig. 1A). The lateral neck lymph nodes (levels IIA, III, IV
and VB) were dissected using the ultrasonic scalpel . After two
drainage tubes being placed, the incision was closed.
The surgical procedure for VALNL group
Patients and methods
Patients and assessments
From March 2013 to December 2014, a total of 58 patients diagnosed with papillary thyroid carcinoma with lateral neck lymph
node metastasis (TNM staging: cN1b) accepted surgical therapies at
the Second Hospital of Shandong University and Qi LU Hospital of
Shandong University. All diagnoses of cN1b-stage, defined as papillary thyroid carcinoma with neck lymph node (levels II, III, IV
and V) metastasis, were confirmed preoperatively by fine needle
aspiration biopsy. No specific exclusion criteria were adopted for this
retrospective study. Before the operation, all patients were informed
about the two surgical methods in detail, and then they chose the
surgical method on their own wish. Patients were divided into two
groups according to the types of thyroid surgery accepted: the
After total thyroidectomy and central neck lymphadenectomy (level VI),
a trocar with a diameter of 5 mm was placed in the skin above
the clavicular head (Fig. 1B, point 2). A rigid 30-degree laparoscope
and some laparoscopic instruments were inserted through the incision located at line 1 (Fig. 1B), and laparoscopic blunt dissecting forceps were inserted into the trocar at point 2 (Fig. 1B). A working
space under the platysma muscle was established (21) and one or
two small s-shaped retractors were used to maintain the operating
space. Its upper border was digastric muscle and its outer border
was musculi trapezius and accessory nerve (Fig. 2). With the amplified dynamic graphs obtained through laparoscope on the monitor
(Fig. 3), the sternocleidomastoid muscle was completely separated
from the strap muscles using the laparoscopic instruments. The carotid sheath was opened subsequently, and then the carotid artery
and the jugular vein were separated gently from the clavicle to the
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637
Figure 1. Illustration of the incision design. (A) The incision design for the conventional lateral neck lymphadenectomy. (B) The incision design for the minimally
invasive video-assisted lateral neck lymphadenectomy. Line 1: The incision for total thyroidectomy and central neck lymphadenectomy. Point 2: The point where
the trocar is placed. Point 3: The point where a special thyroid retractor pierces through the skin to retract the jugular vein.
effective hemostasis and rinsing the operating field, two drainage
tubes were placed in the thyroid and the lateral neck operating field,
respectively. The incisions were closed with absorbable sutures.
All surgical parameters were recorded, including operative time,
length of incision and operative hemorrhage. Some postoperative
parameters, including postoperative drainage, the number of the
resected lymph nodes, the incidence of lymphatic leakage and local
skin paresthesia, the length and cost of hospitalization, were also
recorded. All parameters were compared between the two groups.
In addition, after 1 or 2 months of surgery, the I131 scanning
was performed to check whether metastatic lymph nodes were residual in the lateral neck area.
Statistical analysis
The results were presented as mean ± standard deviation. χ2 test,
Mann–Whitney U test and unpaired t-test were used to evaluate the
statistically significant differences. A P value <0.05 was considered
to indicate a statistically significant difference. Statistical analysis
was performed using SPSS version 19.0 for windows (SPSS, Inc.,
Chicago, IL, USA).
Figure 2. The anatomic landmark to identify the operating space and the dissection area of lateral neck lymph nodes. The gray shadow shows the working place and the bold line on the edge of shadow shows its border, where
the lateral neck lymphadenectomy was made during the minimally invasive
video-assisted surgery.
digastric muscle (Fig. 3A). A special thyroid retractor with a diameter of 2mm (Fig. 4) pierced through the lateral neck skin (Fig. 1B,
point 3) to retract the jugular vein (Fig. 3A,B). The spinal accessory
nerve (Fig. 3B) was identified and traced carefully along its course
until we could see where it passes across the undersurface of the
sternocleidomastoid muscle (Fig. 3A,B). The subplatysmal skin flap
was elevated, and the submandibular gland was exposed and preserved carefully. The omohyoid muscle can be as an important landmark of the lateral neck lymph nodes (Fig. 3A). As the transverse
cervical artery was another anatomy mark (Fig. 3B), all the lymphoid and fat tissues on the surface of the deep fascia could be differentiated easily and dissected completely by the ultrasonic scalpel
(Fig. 3A,B), including levels IIA, III, IV and VB (Fig. 2). Following
Results
Patient characteristics
A total of 58 patients were enrolled in this retrospective study, 30 in
the CL group and 28 in the VALNL group. There was no statistically significant difference between the clinical characteristics of the
two groups (Table 1).
Surgical treatment
Surgical parameters of both the groups are presented in Table 2.
Statistically significant difference was observed in several surgical
parameters. The mean incision length in the VALNL group was 5.2 cm
significantly shorter than 21.4 cm in the CL group. The incidence of
local skin paresthesia in the CL group was 86.67% higher significantly than 28.57% in the VALNL group. There was no significant
difference in operative time, operative hemorrhage, the number of
lateral neck lymph nodes resected and the incidence of lymphatic
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A minimally invasive surgery for thyroid carcinoma
Figure 3. The graph in the period of our minimally invasive video-assisted lateral neck lymphadenectomy. (A) Exposure of lymph nodes of levels III, IV and VB.
(1) Common carotid artery, (2) internal jugular vein, (3) omohyoid muscle, (4) sternocleidomastoid muscle, (5) lymph nodes of levels III, IV and VB and (6) a retractor
for internal jugular vein. (B) The operating space after lymph node dissection was finished. (1) Common carotid artery, (2) internal jugular vein, (3) brachial plexus,
(4) phrenic nerve, (5) transverse cervical artery, (6) cervical plexus, (7) accessory nerve, (8) sternocleidomastoid muscle and (9) a suction and irrigation tube.
surgery, no patients in both groups needed analgesia. No incisional
infection occurred in all cases of both groups. Certain postoperative
complications such as permanent voice change, shoulder dysfunction
and hypocalcemia were not observed as well. I131 scanning result
confirmed that there was no residual metastatic lymph node in the
lateral neck area in both groups. In the follow-up period, no recurrence or metastasis occurred in any of the patients of both groups.
Patients from the VALNL group had more satisfactory cosmetic
results and less scars than those in the CL group (Fig. 5).
Discussion
Figure 4. The special self-made thyroid retractor with 2mm diameter used in
our minimally invasive video-assisted lateral neck lymphadenectomy. The
left semicircle is for hooking by finger. The length of the middle part is
~20 cm, which can be shortened or lengthened to fit for different patients.
The right-angle end is for retracting the jugular vein.
Table 1. Clinical characteristics of the cases
Clinical characteristics
CL group
(n = 30)
VALNL group
(n = 28)
P value
Age (years)
Gender (male/female)
History of surgery in neck (n)
44.80 ± 8.06
11/19
3 (10%)
41.70 ± 7.60
9/19
2 (7.14%)
0.138
0.717
0.936
CL, conventional lymphadenectomy; VALNL, minimally invasive videoassisted lateral neck lymphadenectomy.
leakage. In the VALNL group, the mean length of hospitalization
was 3.40 days shorter than 5.50 days in the CL group, but no significant difference in costs of hospitalization was observed between the
groups.
Treatment outcomes
The postoperative complications including lymphatic leakage and
local skin paresthesia were treated with the conventional method.
The follow-up time ranged from 14 to 32 months. All patients
received I131 radiotherapy 2 or 3 months after the operation. After
The lymph node metastases account for 12–80% of patients with
differentiated thyroid carcinoma (DTC) while diagnosed (22,23),
which is a critical factor of prognosis of patients with DTC following
surgery (24,25). The complete dissection of lateral neck lymph nodes
can increase the survival rate and decrease the recurrence rate in
patients with DTC with lymph node metastases (23,26,27); however, postoperative complications, such as skin paresthesia and conspicuous scar, are frequently observed in patients who have accepted
conventional surgery of thyroidectomy plus lateral neck lymphadenectomy that requires a 15- to 20-cm arc-shaped incision (28). With
the increased incidence of DTC in young people and the improved
long-term cure rate, both patients and surgeons have an increased
demand for a new surgical technique that has less injury and better
cosmetic result.
To our knowledge, minimally invasive video-assisted thyroidectomy was reported firstly to be successfully applied in treating thyroid carcinoma in 1999 (29), and this new technique has become
the most popular minimally invasive thyroidectomy worldwide
(14,30,31). Because of its reduced surgical injury, better wound
healing and better cosmetic outcome, this new technique has been
widely applied in the treatment of thyroid carcinoma and made exciting outcomes (32–35). Although the video-assisted surgical technique has much experience in thyroidectomy and central neck
lymphadenectomy (5,10,13,15,33,36), its application in lateral neck
lymph node dissection has been little reported. Several reports have
presented the example of successful lateral neck lymphadenectomy
using robotic surgical technique (6,16,37,38), but its application has
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639
Table 2. Details of surgical parameters of cases
Surgical parameters
CL group (n = 30)
VALNL group (n = 28)
P value
Operative time (minutes)
Length of incision (cm)
Operative hemorrhage (ml)
Postoperative drainage (ml)
Number of lymph nodes resected (IIA, III, IV and VB regions)
Cases with lymphatic leakage
Cases with local skin paresthesia
Length of hospitalization (days)
Costs of hospitalization (dollars)
210.41 ± 43.54
21.4 ± 5.32
72.30 ± 18.20
153.4 ± 36.1
33.37 ± 7.60
3 (10%)
26 (86.7%)
5.50 ± 1.70
3640.20 ± 482.87
220.8 ± 50.02
5.2 ± 1.6
65.0 ± 16.30
142.9 ± 33.9
30.45 ± 6.05
2 (7.14%)
8 (28.6%)
3.40 ± 1.20
3705.97 ± 388.83
0.402
0.000a
0.114
0.259
0.078
0.936
0.000a
0.000a
0.572
a
Statistically significant difference.
Figure 5. The aspects after the surgery. (A) CL group; (B) VALNL group.
been limited due to the high cost and the special request for the
surgical equipment.
In this study, we introduced a new surgical method of lateral
neck lymphadenectomy using a video-assisted technique. With the
amplified graphs from the laparoscope, the operating field was
exposed very well and the nerves and blood vessels could be identified easily. The appropriate retractors could maintain a good operating space for CO2 insufflation to avoid complications such as
subcutaneous emphysema. Compared to the conventional open surgical method, the new minimally invasive lateral neck lymphadenectomy has a perfect cosmetic outcome of only two small scars left.
Because of the reduced surgical trauma, nerve damage decreased
greatly, which led to the reduction of incidence of complication of
skin paresthesia in the VALNL group. So it was demonstrated that
this new surgical method could improve the postoperative life quality of patients with DTC with lymph node metastases. Meanwhile, it
was determined that our surgical method has adequate security
because the surgical risks were not increased in the VALNL group,
which had similar operative time, operative hemorrhage, postoperative drainage and incidence of lymphatic leakage to CL group.
Though the surgical cost in the VALNL group was higher than that
in the CL group, the more rapid recovery had shortened the length
of hospitalization, so that two groups had similar total cost of
hospitalization.
When the postoperative drainage fluid contains chylous exudate,
triglyceride (TG) test should be conducted. If the TG level in the
drainage fluid was >2.6 mmol/l, the diagnosis of lymphatic leakage
should be considered (39). It was reported that the incidence of lymphatic leakage was 1–2.5% after cervical lymphadenectomy among
the patients with thyroid cancer with cervical lymph node metastasis
(40). In our study, the incidence of lymphatic leakage was frequent
in both groups (10 versus 7.14%), which was significantly higher
than the previous report. The reason might be some small lymph
vessels were not ligatured during the surgery because one of the main
surgical apparatus used in the lateral neck lymphadenectomy was a
harmonic scalpel instead of an electrotome. However, the degree of
lymphatic leakage in both groups was very slight (<100 ml/d). With
the treatments including local pressure bandage, sufficient drainage
and a low-fat diet, all patients with lymphatic leakage were completely
cured, and their length and cost of hospitalization did not increase
significantly.
In this study, our operative range of the lateral neck lymph node
dissection did not include levels IIB and VA. On the one hand, this
area is too far away from the incision. If we tried to remove the
lymph nodes of the two levels, the work space must extend across
the spinal accessory nerve that results in the increased risk of nerve
damage. On the other hand, the lymph node metastases in DTC
were rarely observed to levels I, IIB or VA (41,42). In some rare
cases with the lymph node metastases with levels IIB and VA, I131
radiotherapy after operations could benefit a long-term survival and
decreased the recurrence rate. For these reasons, we defined that the
usual range of lateral neck lymph nodes dissection are levels IIA, III,
IV and VB in VALNL. The surgical outcomes in VALNL was satisfactory. There was no significant difference in the number of lymph
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A minimally invasive surgery for thyroid carcinoma
nodes resected in both groups, and no residual metastatic lymph
node was found in all subjects. After a follow-up period of >1 year,
all patients were still disease-free. Certain reports showed that the
DTC cells could implant and develop in the operating field due to
the laparoscopic surgery (43,44). This situation had never happened
to our patients. Unlike the robotic surgical technique, our method
does not request special expensive equipment, which can be applied
more easily and widely in the clinical treatment of patients with
DTC. Notwithstanding the advantages of less postoperative complications and better cosmetic outcome, it still needs to further investigate the survival benefit of the minimal invasive VALNL and
determine more therapeutic paradigm for patients with DTC with
cervical lymph node metastases.
The new minimally invasive surgery, VALNL, is a feasible and
safe alternative for the treatment of thyroid carcinoma with cervical
lymph node metastases. It provides a better treatment choice than
conventional thyroid surgery. Further investigation will involve
more cases and perform a longer follow-up period to test the possibility of this new surgical method to replace the conventional open
surgery in patients with thyroid carcinoma with cervical lymph node
metastases.
Funding
This study was supported by the Seed Fund of the 2nd Hospital of
Shandong University (grant no. S2015010007) and the Special Ally
Project of Natural Science Foundation of Shandong Province (grant
no. ZR2014HL060).
Conflict of interest statement
None declared.
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