Journal of Robotic Surgery (2020) 14:317–323

https://doi.org/10.1007/s11701-019-00986-3

ORIGINAL ARTICLE

Robotic lateral cervical lymph node dissection via bilateral

axillo‑breast approach for papillary thyroid carcinoma: a single‑center
experience of 260 cases
Qingqing He1 · Jian Zhu1 · Dayong Zhuang1 · Ziyi Fan1 · Luming Zheng1 · Peng Zhou1 · Fang Yu1 · Gang Wang1 ·
Gaofeng Ni1 · Xuefeng Dong1 · Meng Wang1 · Xiaolei Li1 · Changrui Liu1 · Dan Wang1 · Tao Yue1 · Lei Hou1 ·
Mengdi Wang1 · Dandan Li1

Received: 22 October 2018 / Accepted: 6 June 2019 / Published online: 20 June 2019
© The Author(s) 2019

Abstract
To evaluate the feasibility and safety of robotic lateral cervical lymph node dissection via BABA, 260 thyroid cancer patients
with suspected level II, III, IV, and ­Vb lymph node metastasis were selected. The lateral cervical compartment was exposed
by splitting the sternocleidomastoid muscle longitudinally, and separating between the strap muscles and the anterior margin
of the sternocleidomastoid muscle. The procedure was completed in 260 patients. Mean time for robotic lateral node dissec-
tion took 80 ± 21 min. The wound catheter was removed 6.3 days. Postoperative transient symptomatic hypocalcemia was
observed in 51 patients, transient hoarseness in three, seroma in three, chyle leakage in two, and tracheal injury in one. 124
patients were confirmed to have lymph node metastasis on final pathological report. Average postoperative hospital stay was
6.5 days. Robotic lateral neck dissection by BABA is the acceptable operative alternative for thyroid cancer patients who
wished to keep their surgical history private.

Keywords  Papillary thyroid carcinoma · Robotic thyroidectomy · Bilateral axillo-breast approach · Robotic lateral cervical
lymph node dissection

Introduction bilateral central/lateral cervical lymph node dissection (lev-

els II, III, IV, and ­Vb) effectively, without sacrificing surgical
It was George W. Crile who was the first to describe radical safety parameters [4–7]. However, robotic lateral cervical
neck dissection in 1906. Recent innovation in the surgical lymph node dissection remains at an early stage, and further
technique of thyroidectomy has offered the opportunity for evaluations are required.
the patients to stay away from these prominent neck incision
scars. Especially, with the advent of robotic surgical system
(Intuitive Surgical, Sunnyvale, CA), many have adopted the Methods
concept of remote-access surgery and developed various
robotic thyroidectomy techniques [1–3]. Patient eligibility and study design
In China, bilateral axillo-breast approach (BABA) was
utilized in most cases of robotic total thyroidectomy. BABA Since January 2014, we have completed 800 cases of
robotic thyroidectomy makes four tiny incisions (5–12 mm) robotic thyroidectomy. Here, we present our experience of
at areolae and skin creases of the axillae, and can perform 260 patients who received robotic total thyroidectomy with
lateral cervical lymph node dissection via BABA between
Jun 2014 and May 2018. General clinical information of the
* Qingqing He patients is outlined in Table 1.
[email protected] The inclusion criteria for robotic total thyroidectomy with
1 lateral cervical lymph node dissection via BABA were as
Department of Thyroid and Breast Surgery, 960th Hospital
of the People’s Liberation Army, No. 25 Shifan Road, follows: (1) patients of papillary thyroid cancer with suspi-
Jinan 250031, People’s Republic of China cious or cytologically confirmed lateral neck metastasis (by

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Table 1  Clinical characteristics and surgical outcomes of the patients

Items RLCLND (n = 260)

Mean age (years) 41.2 ± 11.9

Male/female, (n) 63:197
BMI (kg/m2) 23.9 ± 3.7
Primary tumor size (mm) 10.7 ± 6.9
Multicentricity/multifocality (n) 97
Type of surgery
 Total thyroidectomy with lateral RLCLND (n) 239
 Total thyroidectomy with bilateral RLCLND 21
(n)
Conversion to open surgery 0
Total number of removed lateral nodes (n) 17.9 ± 8.6
Lateral node metastasis (n) 124
Total operating time (min) 201 ± 63
Postoperative hospital stay (d) 6.5 ± 2.6 Fig. 1  Drawing the instrument arm trajectory lines
Mean drain days (d) 6.3 ± 1.1
Postoperative complications
internal jugular vein or liquefied lymph nodes, or (4) the
 Postoperative bleeding (n) 0
suspicious lymph nodes are located beneath the clavicle.
 Subcutaneous emphysema 0
To assess the extent of disease, neck ultrasonography with
 Pneumomediastinum 0
fine-needle aspiration, neck CT, MRI, or PET-CT was per-
Hypoparathyroidism
formed as preoperative evaluation. All patients were given
 Temporary (n) 51
full information of the possible treatment options for their
 Permanent (n) 0
thyroid cancer, including the advantages and disadvantages
RLN paralysis
of conventional open transcervical approach and robotic sur-
 Temporary (n) 3
gery via BABA, and provided written, informed consents
 Permanent (n) 0
before the surgery.
Seroma 3
The day before robotic surgery, 0.1–0.2 ml of carbon
Skin burn 0
nanoparticles’ suspension injection (Chongqing Lummy
Flap necrosis 0
Pharmaceuticals, China) was injected into the thyroid gland
Hematoma 0
under the guidance of ultrasound, in the purpose of leaving
Tracheal fistula 1
the parathyroid glands unstained, while staining the lymph
Wound infection 1
nodes of the center compartment and lateral cervical [5].
Chyle leakage (n) 2
Postoperative Tg level (ng/mL) 0.81 ± 0.2
Surgical procedures
Cosmetic satisfaction score 4.68 ± 0.35
Mean follow-up (months) 28.6 ± 8.3
Position
BMI body mass index, RLN recurrent laryngeal nerve, Tg thyroglobu-
lin, RLCLND robotic lateral cervical lymph node dissection Under general endotracheal anesthesia, patient was placed
on the operating table in the supine position with the neck
slightly extended and both arms slightly abducted to allow
FNAC), central lymph node metastasis (diagnosed by frozen insertion of the axillary port. After draping, we draw the
section examination during the operation), or evident lateral instrument arm trajectory lines and working area on patient’s
neck lymph node metastasis on preoperative imaging stud- chest and neck for reference (Fig. 1).
ies and (2) patients with no previous history of treatment
for neck surgery of any kind, whereas the exclusion criteria Flap design and dissection
were: (1) metastatic lymph nodes were fused with each other
or fixed in the neck, or (2) patients with thyroid carcinomas Draw guidelines along the landmarks of the chest and the
that showed gross invasion to local structures or extensive neck, such as the linea alba, trachea, thyroid cartilage, cri-
extrathyroidal capsular spread (such as trachea, esophagus, coid cartilage, anterior border of the sternocleidomastoid
and recurrent laryngeal nerve), or (3) patients with the met- (SCM) muscle, the clavicles (Fig. 2), suprasternal notch,
astatic lymph nodes encase the common carotid artery or circumareolar and axillary incisions, and trajectory lines

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Journal of Robotic Surgery (2020) 14:317–323 319

created, the lateral cervical compartment was exposed by

splitting the SCM longitudinally and separation between
the strap muscles and the anterior margin of the SCM is
needed. The entire medial border of the SCM muscle is dis-
sected with lateral traction of the Maryland forceps. The
omohyoid muscle is identified and protected, and its infe-
rior belly is dissociated by a Harmonic curved shear. The
omohyoid muscle is lifted upward and the internal jugular
vein is revealed. The omohyoid muscle is retained during
the operation to maintain the appearance of the lateral area
(Fig. 2). After the medial border of SCM is fully exposed,
the muscle is pulled laterally using small gauze roll by 5 mm
Maryland dissector.
Fig. 2  Surgical landmarks of lateral neck node
Lateral cervical lymph node dissection

The lateral cervical compartment was exposed by splitting

SCM longitudinally, and separating between the strap mus-
cles and the anterior margin of SCM. One should notice
that the harmonic scalpel has a limited range of motion and
lacks side-bending capabilities; at the same time, the camera
is not flexible and the surgical view is limited. For better
visualization the lowermost sub-clavicular area, the robotic
30° down camera is set as possible as high. A slight clock-
wise or counterclockwise rotation of the camera port is also
recommended. The internal jugular vein is drawn medially
using the Prograsp forceps. The soft tissue with lymph nodes
is detached from the anterior surface of the internal jugular
Fig. 3  Omohyoid muscle and the clavicles were revealed vein to the posterior aspect of the internal jugular vein until
the common carotid artery and vagus nerve are identified.
Inferior dissection of level IV is performed with preservation
from the incision to cricoid cartilage as described in the of the transverse cervical artery and the phrenic nerve. Espe-
previous chapter [2, 5]. cially, in the left level IV dissection, branches of the thoracic
Usually, 5 mm Maryland dissectors are docked in the left duct are identified by the 15 times magnified view of the da
axillary port, and the Prograsp forceps are docked in the Vinci Si system. Thoracic duct needs to be preserved. Main
right axillary port. Maintain low pressure (5–6 mmHg) with trunk of the thoracic duct can be ligated using absorbable
high flow of carbon dioxide (15 l/min) to create surgical sutures or robotic Hem-o-lok clips to prevent postoperative
field. The working space for BABA robotic lateral neck dis- chyle leakage. Small branches of lymphatic ducts can be
section should be made wider than the flap for usual robotic managed using harmonic curved shears. Careful dissection
thyroidectomy. It should be extended over the lateral bor- of level IV is required to preserve the phrenic nerve. Do not
der of the ipsilateral SCM muscle laterally and to the lower injure the phrenic nerve which is always deep to the trans-
border of the submandibular gland and posterior belly of verse cervical artery, do not enter the deep space beneath
digastric muscle superiorly. It is important that sufficient the transverse cervical artery unless absolutely necessary.
working space can be created for comfortable movements The dissection is extended to level III after dissecting
of the robotic arms through the BABA during both total level IV and ­Vb. The vagus nerve and the phrenic nerve that
thyroidectomy and neck dissection. During flap dissection to are identified at the level IV dissection should be traced care-
the lateral side, identifying and protecting the great auricular fully not to pose any injury. Care should be taken to preserve
nerve are also of vital importance. C2, C3, and C4 as far as possible (Fig. 3). Dissection of the
After completing total thyroidectomy and central com- level III compartment is performed carefully not to perforate
partment dissection, dissection of ipsilateral or bilateral the internal jugular vein.
levels II, III, IV, and ­Vb was performed (Fig. 3). The steps IIa and III compartments were exposed by separating
of robotic lateral cervical node dissection were similar to between the strap muscles and the anterior margin of SCM.
those of conventional surgery. After the working space was The dissection proceeds until the posterior belly of the

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320 Journal of Robotic Surgery (2020) 14:317–323

digastric muscle is exposed superiorly. The spinal accessary

nerve runs under the internal jugular vein mostly, but can be
found over the internal jugular vein sometime, and should
be preserved at this point. The spinal accessary nerve can be
confirmed with the current of 3.0–5.0 mA of neuromonitor
(Shanghai NCC Medical Co., LTD, China).

Closure

The resected specimen was extracted through enlarging the

axillary skin incision using a specimen pouch. Meticulous
hemostasis is needed. The surgical area was irrigated by
3500 ml sterile distilled water (42 °C) to reduce tissue debris Fig. 4  Ultrasonic scalpel burning tracheal wall
to prevent tumor tissue planting. Suture the linea alba is
needed in most cases. One vacuum-assisted draining system
is inserted in levels IV area though ipsilateral axilla tunnel,
and the other one should be placed in the thyroid bed though
the areolar tunnel. The skin incision was closed with 5–0
absorbable sutures using an atraumatic needle, and wounds
are covered by placement of Steri–Strips. The drains are
removed when the patient is discharged, usually on postop-
erative days 4–7.

Statistical analysis and followed up

For descriptive statistics of quantitative variables,

mean ± standard deviation and range were used to describe
central tendency and dispersion. For analysis of the differ-
ences in proportions was used. Follow up by outpatient,
phone, email, and WeChat. Tumor recurrence is regularly
monitored by ultrasonography (ultrasound and ultrasound- Fig. 5  Tracheal fistula and tracheal annular stenosis
guided fine-needle aspiration citology), measuring Tg or
FNA-Tg concentration at the outpatient clinic. Neither iat-
rogenic implantation nor metastasis occurred in drain tract/ 2 months. Chyle leakages were managed conservatively with
chest wall was found by inspection or ultrasound during a fat-free diet and by placing a compressive dressing over the
follow-up. supraclavicular fossa without the need for further surgical
Cosmetic satisfaction at 3 months postoperatively was intervention, symptom resolved within 2 weeks. There are
assessed using a five-point scale (extremely satisfied, satis- three patients with RLN paralysis, and this was determined
fied, acceptable, dissatisfied, or extremely dissatisfied). on laryngoscopy.
Lateral cervical lymph node dissection (unilateral or bilat-
eral levels II, III, IV, and V
­ b) via BABA was completed suc-
Results cessfully in 260 patients without any significant intraopera-
tive complications or conversion to open/other approaches
All the patients received thyroid hormone replacement (Table 1). Mean operative time was 201 ± 63 min, in which
therapy for life-long time. All complications were recorded, mean console time for robotic lateral neck dissection took
including one patient who had severe scar constitution 80 ± 21 min. The wound catheter was removed 6.3 ± 1.1 days
underwent tracheal fistula 5  days after surgery (Fig.  4). after surgery. This series was comprised of patients [(body
During the operation, thyroid cancer was found to infiltrate mass index, BMI): 20–37.7 kg/m2, average 23.9 ± 3.7 kg/
the trachea, and ultrasonic knife was used to cauterize the m2] with thyroid nodules (average 12 mm) across all age
infiltrated tracheal wall (Fig. 4), which was managed con- groups (41.2 ± 11.9 years, range 15–68 years). Majority of
servatively without the need for further surgical interven- patients (n = 146,56.2%) had papillary thyroid microcar-
tion (Fig. 5). All cases of transient hypocalcemia resolved cinoma on final surgical pathology, rest 43.8% had papil-
with the need for calcium or vitamin D supplementation in lary thyroid cancer. In this study, postoperative transient

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symptomatic hypocalcemia was observed in 51 patients 2016, the American Thyroid Association again published a
(19.6%), postoperative transient hoarseness in 3 (1.15%), statement, indicating that remote-access thyroidectomy may
seroma in 3 (1.15%), chyle leakage in 2 (0.7%), and tracheal be performed safely in high-volume centers [15], and there
fistula (caused by ultrasonic knife cauterization) in 1 (0.4%) acknowledged the role of robotic thyroidectomy in selected
(Figs. 4, 5). There was no permanent hypocalcemia and patients and emphasized the importance of strict selec-
hoarseness, no pneumothorax or carotid artery injury, and no tion criteria [14–16]. The selection of approach is largely
traction injury. No bleeding or hematoma was encountered. dependent on the training, skill, and preference of the sur-
No implantation or metastasis occurred in drain tract or chest geon and/or patient [17].
wall. 124 patients (47.7%) had lymph node metastasis in Compared to the conventional open approach, robotic
the lateral compartment confirmed on the final pathological total thyroidectomy with lateral cervical lymph node dis-
report. Mean lymph node yield in the lateral compartment section only requires one 1.2 cm and one 0.8 cm incisions
was 17.9 (17.9 ± 8.6, range 7–41). Average postoperative in bilateral areolas, one 0.8 cm and one 0.5 cm incisions
hospital stay was 6.5 ± 2.6 days (range 3–11 days). at the axillary crease. These wounds could be well-hidden
All patients are being followed up (average with everyday clothing, which was especially important in
28.6 ± 8.3 months, range 1–48 months) on a regular basis. patients who wished to keep their surgical history private.
All cases experienced sensory impairment in the neck, The essence of robotic thyroidectomy by BABA entails
chest, or the nipples after BABA procedures, but such touch better patients’ satisfaction on cosmetic outcomes. Appro-
and pain disturbance could be normalized completely by priate positioning of the patient and configuration of the
4–12 months. Cosmetic satisfaction score was 4.68 ± 0.35. robotic instruments are keys to successful operation. It is
No patient who had issues with postoperative paresthesias, important that sufficient working space be created for com-
pain, breast asymmetry, the brachial plexus injuries, or neck fortable movements of the robotic arms through the axil-
stiffness. lary–areolar ports during both total thyroidectomy and neck
In one 27-year-old male patient’s 13 months postopera- dissection. In comparison with traditional transcervical open
tively ultrasound examination, swollen lymph nodes on the methods, by placing the surgical incision in the axillary
left side of the level IV were revealed with serum Tg less and circumareolar, an obvious cervical incision would be
than 0.2 ng/mL. The combination of FNAC and FNA-Tg completely refrained. Robotic thyroidectomy system com-
(eluent Tg > 300 ng/mL) diagnosed lymph node metastasis bines the unique benefits of the surgical robot and remote-
and the patient received open surgery later to remove one access thyroidectomy provides the welfares of excellent
metastasis lymph node. 118 patients have received high- 3-D visualization,stable and magnified operative view, and
dose (104–150 mCi) radioiodine ablation therapy after the improved surgical dexterity. It has been proved to have com-
operation. parable surgical safety and oncological completeness with
traditional open operation, and creates smaller injury (psy-
chological and physical injury), better functional preserva-
Discussion tion (including neck function, parathyroid glands, and laryn-
geal nerve), and significantly cosmetic satisfaction. Indeed,
The most commonly used approaches are BABA in China many patients are highly concerned on the scar associated
[5–7], the symmetry of the BABA system enables bilateral with thyroid surgery and with the difficulty hiding this scar.
central/lateral neck dissection. Other new approaches to At present, the amount of Chinese community medical insti-
robotic thyroidectomy also have been described, including tutions and family care physicians cannot meet the need of
axillary breast, retroauricular, and transoral [8–12]. The individual patients’ postoperative follow-up treatment, and
BABA is a multidirectional approach in which the midline is most thyroid cancer patients stay in hospital after surgery
the viewpoint, whereas the other ones are lateral approaches. until the removal of the neck drainage pipe discharge. There-
Majority of patients had microcarcinoma, yet all had lat- fore, postoperative hospital stay usually was 6 days. Late
eral neck node dissection, with overall only 47.7% small follow-up results indicated that splitting the SCM longitu-
positive nodes in the specimen. With such low yield, most dinally during neck dissection did not increase postoperative
of the neck dissections were done prophylactically. How- pain and morbidity, such as neck stiffness (especially with
ever, most microcarcinomas would only require lobectomy bilateral procedure).
and rarely need prophylactic central neck node dissection Using convenient robotic instruments helped to overcome
and none would need prophylactic lateral neck dissection some of the limitations of the endoscopic procedures such as
[13, 14]. It is recommend in China to perform prophylactic reduced range of motion, long and rigid instruments, chop-
central neck node dissection, which is discourage by 2015 sticks effect, and impaired eye–hand coordination (while
ATA guidelines. Prophylactic lateral neck node dissection relying on an unstable 2D view). Robotic thyroidectomy
is specifically discouraged by the ATA guidelines [13]. In has become increasingly popular around the world attracting

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322 Journal of Robotic Surgery (2020) 14:317–323

both surgeons and patients searching for new and innovative but such sensory disturbance could be normalized com-
procedures and allowing for the removal of thyroid with an pletely by 4–12 months. Through technical reinforcement
excellent cosmetic result when compared to the open thy- along with experience accumulation and development of
roidectomy. Many reports have described the safety of the robotic instruments, robotic thyroidectomy can overcome
remote-access robotic thyroidectomy procedures and have the possible limitation of safety and oncological radical-
demonstrated comparable oncologic outcomes between the ness and can also be a new treatment modality for papillary
robotic and open thyroidectomy [12, 16]. thyroid cancer. In addition, guidelines are needed to reduce
From surgeon’s point of view, the bilateral axillo-breast trial errors [17].
approach would be more comfortable due to familiar local
anatomical structures, easier to address the thyroid gland,
trachea, recurrent laryngeal nerve, and the spinal acces- Conclusions
sory nerve, and lymph node tissues at the central or bilat-
eral cervical lymph node could be easily reached due to the Robotic thyroidectomy is not for every patient, surgeon, or
decreased area of dissection compared with the transaxil- hospital. Considered and measured patient selection is para-
lary, transoral, or retroauricular approach [16]. BABA most mount. Robotic thyroidectomy with lateral cervical lymph
closely resembles traditional thyroid surgery, as it provides node dissection via BABA may be an appropriate option for
a midline access to the symmetrical view of both lobes. the carefully selected patients who are committed to com-
Adopting carbon nanoparticles in negative development of pletely avoiding a neck scar.
the parathyroid gland helps to identify and protect the para-
thyroid glands and remove more lymph nodes and shorten
the operation time. This operative procedure, however, has Funding  This study was supported by the grants from the President
disadvantages of longer operation times, use of C ­ O2 insuffla- Funding of Jinan Military General Hospital of PLA (No. 2013 ZD 05
and No. 2016 ZD 02).
tion, no force and haptic feedback, and the higher costs. It is
contemplated that the operation time would be significantly
Compliance with ethical standards 
decreased through accumulation of surgical experience. The
insufflation of high volume of carbon dioxide (15 l/min) to Conflict of interest  Qingqing He, Jian Zhu, Dayong Zhuang, Ziyi Fan,
maintain low pressure (5–6 mmHg) can obtain satisfactory Luming Zheng, Peng Zhou, Fang Yu, Gang Wang, Gaofeng Ni, Xue-
surgical field, and can avoid the occurrence of subcutaneous feng Dong, Meng Wang, Xiaolei Li, Changrui Liu, Dan Wang, Tao
emphysema. Tracheal injury rate was reported in one patient. Yue, Lei Hou, Mengdi Wang, and Dandan Li declare that they have no
conflict of interest.
Tracheal fistula is an uncommon complication. It is some-
thing to be concern about with this approach. The reason for Ethical standards  All procedures followed were in accordance with the
consideration is that in the case of patients with severe scar ethical standards of the responsible committee on human experimenta-
constitution and lack of haptic feedback, severe burning of tion (institutional and national) and with the Helsinki Declaration of
1975, as revised in 2000.
the trachea by ultrasonic knife leads to tracheal wall necrosis
and tracheal fistula. However, most experienced surgeons Informed consent  Informed consent was obtained from all patients for
may compensate for this drawback using visual thinking. being included in the study.
Despite all progress, the financial commitment and time
sacrifice are the major limitations for a broad implementa- Open Access  This article is distributed under the terms of the Crea-
tion of robotic thyroidectomy into daily routine. Despite our tive Commons Attribution 4.0 International License (http://creat​iveco​
promising operative results, an expanded population from mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribu-
tion, and reproduction in any medium, provided you give appropriate
careful selection of eligible patients is mandatory, and future credit to the original author(s) and the source, provide a link to the
prospective trials should be conducted to evaluate long-term Creative Commons license, and indicate if changes were made.
outcomes and to overcome potential limitations [17–24].
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