Oral Oncology 71 (2017) 75–80

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Oral Oncology
journal homepage: www.elsevier.com/locate/oraloncology

Transoral thyroidectomy and parathyroidectomy – A North American

series of robotic and endoscopic transoral approaches to the central neck
Jonathon O. Russell a,⇑, James Clark a, Salem I. Noureldine a, Angkoon Anuwong b, Mai G. Al Khadem a,
Hoon Yub Kim c, Vaninder K. Dhillon a, Gianlorenzo Dionigi d, Ralph P. Tufano a, Jeremy D. Richmon a
a
Division of Head and Neck Endocrine Surgery, Department of Otolaryngology – Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA
b
Minimally Invasive and Endocrine Surgery Division, Department of Surgery, Police General Hospital, Siam University, Bangkok, Thailand
c
Department of Surgery, Minimally Invasive Surgery and Robotic Surgery Center, KUMC Thyroid Center, Korea University, Anam Hospital, Seoul, Republic of Korea
d
Division of General Surgery, Research Center for Endocrine Surgery, Department of Surgical Sciences and Human Morphology, University of Insubria, Varese, Italy

a r t i c l e i n f o a b s t r a c t

Article history: Objective: Most thyroid surgery in North America is completed via a cervical incision, which leaves a per-
Received 6 March 2017 manent scar. Approaches without cutaneous incisions offer aesthetic advantages. This series represents
Received in revised form 3 May 2017 the largest series of transoral vestibular approaches to the central neck in North America, and the first
Accepted 2 June 2017
published reports of robotic transoral vestibular thyroidectomy for thyroid carcinoma.
Available online 10 June 2017
Materials and methods: Data was prospectively collected for patients that underwent transoral vestibular
approach thyroidectomy and/or parathyroidectomy between April 2016 and February 2017.
Keywords:
Results: Fifteen patients underwent the procedure for removal of the thyroid (n = 12), parathyroid (n = 2)
Robotic thyroidectomy
Robotic parathyroidectomy
or both thyroid and parathyroid glands (n = 1). The first case was converted to an open procedure.
Endoscopic thyroidectomy Fourteen were completed through these remote access incisions, including patients with a body mass
Minimally invasive index as high as 44. There were no permanent complications. The postoperative median Dermatology
Transoral thyroidectomy Life Quality Index score was 3, which indicates a small effect on quality of life.
Transoral endoscopic thyroidectomy Conclusion: The transoral vestibular approach to the central neck is a promising technique for patients
vestibular approach who desire to optimize aesthetics.
TOETVA Ó 2017 Elsevier Ltd. All rights reserved.
TORT
TONS

Introduction ent thyroidectomy techniques have been proposed as alternatives

to the conventional transcervical incision, but none has gained
Since its description by Kocher in the late 1880’s, the transcer- prominence or been widely adopted in a Western population
vical incision has constituted the primary surgical approach to the [8,9]. Each represents surgical compromise between exposure
thyroid and parathyroid glands [1]. The utility of this incision and aesthetics, necessitating either a small but visible scar [10]
design is clear, as it provides the surgeon with excellent exposure or extensive tissue dissection with a remote, hidden scar
and a direct route to the central neck. Despite meticulous closure [11–18]. Application of these techniques to Western patients with
of the incision, a scar of variable prominence is inevitable and a higher body mass index (BMI) has also been difficult in some
patients can find it disagreeable [2–4]. cases [5].
The increasing incidence of thyroid pathology, the young aver- To address these concerns, authors have previously attempted
age age at presentation, a female predominance, and a societal transoral approaches [7]. A transoral vestibular approach avoiding
emphasis on physical appearances have provided impetus to the floor of mouth was described by Richmon et al. [19], and mod-
develop aesthetically favorable alternative approaches [5,6]. Mini- ifications of this technique have gained favor particularly in Asia,
mally invasive surgery and remote access approaches are alterna- where it continues to evolve with refinement of incision placement
tive methods that respect surgical planes, minimize surgical [20,21]. When contrasted with other remote access approaches,
trauma and avoid visible scarring [7,8]. Since 1997, over 20 differ- the transoral vestibular approach offers the potential for limited
dissection and a completely hidden incision. Here, we describe
⇑ Corresponding author at: Department of Otolaryngology – Head and Neck our experience using the transoral vestibular approach for thy-
Surgery, The Johns Hopkins School of Medicine. Johns Hopkins Outpatient Center, roidectomy and parathyroidectomy in a Western population. To
601 N. Caroline Street, 6th floor, Baltimore, MD 21287, USA. our knowledge, this single institution series represents the largest
E-mail address: jrusse41@jhmi.edu (J.O. Russell).

http://dx.doi.org/10.1016/j.oraloncology.2017.06.001
1368-8375/Ó 2017 Elsevier Ltd. All rights reserved.
76 J.O. Russell et al. / Oral Oncology 71 (2017) 75–80

patient cohort reported in the Western Hemisphere, and the first to Postoperative care
report robotic assistance. It is also the first to report robotic assis-
tance via a transoral approach for a known thyroid carcinoma. All patients are discharged home within 23 h with a 5-day
course of Augmentin (875 mg twice daily), and clindamycin
(300 mg three times daily) is substituted if allergic to penicillin.
Materials and methods It is our practice to complete the first postoperative follow up for
all patients 5–14 days from surgery (Fig. 3), at which time a flexible
Study population fiberoptic laryngoscopy is again performed to evaluate vocal fold
function. Patients also completed the Dermatology Life Quality
All cases were performed at the Johns Hopkins Hospital Index (DLQI) survey at this visit, at each subsequent visit, and again
between April 2016 and February 2016 by the Head and Neck at 6 months [22]. The DLQI survey has 10 questions with each con-
Endocrine Surgery team, and data was collected prospectively. taining a score of 0–3; a maximum possible score of 30 indicates
Patients were offered a transoral vestibular approach if they had dermatologic issues resulting in severely impaired quality of life.
a history of hypertrophic scarring or were otherwise motivated In our series, the first and the last DLQI from each patient were
to avoid a cervical incision, did not have a known history of thy- used to calculate the mean and median.
roiditis or external beam radiation, and had a thyroid nodule that
was smaller than 6 centimeters (cm) on preoperative ultrasound.
Informed consent was obtained from all patients, including a Results
review of the novel nature of this procedure and the associated
risks. Patients were offered robotic or endoscopic transoral A total of 15 transoral vestibular approaches were attempted
vestibular approaches as per robot availability, with no set criteria between April 2016 and February 2016: Six of these cases were
being established to differentiate between the two groups. The for cytologically benign thyroid nodules, five were for indetermi-
procedure was approved by the operating room privileging com- nate thyroid nodules, two were for parathyroid adenomas, one
mittee as well as risk management. Johns Hopkins Institutional was for papillary thyroid carcinoma, and one was for both a
Review Board approval was obtained to review the collected data. parathyroid adenoma and an indeterminate behavior thyroid nod-
ule. The first case was converted to an open procedure, but all of
the subsequent 14 cases were successfully completed without a
Surgical technique cervical incision. The characteristics of all patients who completed
the transoral vestibular approach are summarized in Table 1. The
The surgical approach is based on the technique described by BMI ranged from 19.9 to 44, with a median of 28 and a mean of
Anuwong [20]. The patient is positioned supine and intubated with 30.3. The papillary thyroid carcinoma was unifocal with a size of
a 6-0 nerve monitoring endotracheal tube (Medtronic, etc). A 1.3 cm, and final pathology demonstrated negative margins.
1.5 centimeter (cm) incision is marked out in the midline of the Of the 14 transoral vestibular surgeries, six (42.9%) were per-
lower lip at approximately 1 cm above the gingivobuccal sulcus formed using the da Vinci Si robot (Intuitive Surgical, Inc, Sunny-
(Fig. 1A). Electrocautery and blunt dissection are then used to vale, CA) and eight (57.1%) were performed with endoscopic
approach the mandible. Once the periosteum is identified, the neck instrumentation alone (Table 2). The first three specimens
is injected with 1:500,000 epinephrine using a fat injection syringe. (21.4%) were divided within the specimen bag to facilitate delivery
Next, a dilator is used to develop the submental and subplatysmal via the transoral incision, while the remainder were removed en
plane bluntly in the midline. Lateral stab incisions are made and bloc. The median maximal dimension of the removed thyroid lobes
injected with the epinephrine solution at the lateral aspect of the was 6.5 cm (range 2.6–6.5 cm). The median operative time was
lower lip (Fig. 1C). The endoscopic ports are brought into the field 288.5 min (range 189–448 min). The first procedure took
and insufflation begins at a pressure of 5–7 mmHg (Fig. 1D). 322 min, while the last took 189 min. Robotic procedures had a
The subplatysmal pocket is developed with endoscopic instru- median duration of 344 min (range 287–448 min), while endo-
mentation to the level of the sternum and laterally to the stern- scopic procedures required a median of 235 min (range 189–
ocleidomastoid muscles. When utilized, the robot is docked and 343 min). Surgical drains were used in 3 of 14 patients (21.4%).
used for the remainder of the surgery; otherwise, the surgery pro- One (7.2%) of the fourteen patients was discharged on the same
ceeds with endoscopic visualization. The median raphe of the strap day, while the remaining 13 (92.8%) were discharged within
muscles is identified and divided. The thyroid isthmus is divided 23 h. Only one intrathyroidal parathyroid was identified in the
and the trachea serves as a landmark for identification of the 12 thyroid lobectomies completed. Estimated blood loss was min-
RLN. A capsular dissection begins around the thyroid itself and imal in all 14 cases. The recurrent laryngeal nerve was visually
the superior pole is taken down with the Harmonic scalpel. The identified, stimulated and formally dissected in 5 cases (35.7%).
nerve stimulator probe is used to stimulate the RLN and to test Five patients (35.7%) with benign nodules had the nerve protected
neurophysiologic integrity during and after the procedure. The anatomically by leaving a cuff of normal thyroid at Berry’s
parathyroid glands are readily appreciated if they are in the capsu- ligament.
lar plane. A parathyroid adenoma may also be removed in a similar Table 3 shows the DLQI scores for 14 patients. The median and
fashion. mean DLQI scores were 3 and 3.9 (out of a possible 30), respec-
The RLN is dissected distally after identification as it proceeds tively, corresponding to minimal effect. The score was lower on
laterally and caudally from the point of insertion. The thyroid is subsequent administrations of the survey in all cases in which
delivered off of the trachea. The contralateral lobectomy can be the questionnaire was administered more than once.
completed via the same incisions if necessary [20]. The specimen No patients had permanent complications. One (7.1%) robotic
is retrieved via the central incision using an endocatch bag procedure was converted to an endoscopic approach, with the thy-
(Fig. 2A). Hemostasis is achieved and the wound is irrigated. The roid lobe removed via the transoral incision. Post-operatively, one
oral vestibule incisions are closed with layered absorbable sutures. patient (7.1%) had self-limiting numbness over the mental nerve
A compression dressing is placed across the neck and chin after the lasting for less than 1 month. One (7.1%) patient had a temporary
patient has been extubated. Flexible fiberoptic laryngoscopy is left vocal fold palsy and underwent injection medialization before
completed to confirm vocal fold function. regaining full vocal fold function within 3 months of surgery. Our
 J.O. Russell et al. / Oral Oncology 71 (2017) 75–80 77

Fig. 1. a) A 1.5 cm incision is marked out in the midline at approximately the distal aspect of the buccal frenulum. b) The incision is infiltrated with lidocaine and epinephrine
before making a 1 cm incision with a scalpel. c) Stab incisions are next made at the lateral aspect of the lower lip and infiltrated as above. d) The ports are placed.

Fig. 2. a) One of the thyroid lobes retrieved using a trans oral approach. b) Patient neck immediately at end of transoral thyroid lobectomy.

index case was converted to an open approach due to a substernal assisted thyroidectomy. Furthermore, it is the first report of a
and retroesophageal location that was not recognized on preoper- North American series to use the transoral vestibular approach
ative ultrasound. This patient was not included in the data listed for a known papillary thyroid carcinoma. Finally, this series is the
above. first to report objective quality of life data documenting the mini-
mal impact of the vestibular incisions on quality of life. This
Discussion approach is unique in that it completely avoids a cervical incision.
It can be safely completed on obese populations without perma-
This is the largest North American series of transoral vestibular nent complications. It has multiple advantages over other
approaches to the central neck, and the first report of robot remote-access approaches to the thyroid including less tissue
78 J.O. Russell et al. / Oral Oncology 71 (2017) 75–80

Fig. 3. a) Demonstrates a postoperative mucosal incision site 9 days after surgery. b) Demonstrates a neck 1 month postoperatively.

Table 1
Summary of patient characteristic of pathology and size of the thyroid nodules.

Case no. Gender Age (years) BMI Laterality Pre-operative cytology Pre-operative size of specimen on Imaging (cm) Pre-operative nodule size
1 Female 53 44 Left Adenomatoid nodule 5.3  2.3  3.2 3.5
2 Female 17 36 Left AUS 5.3  2.5  3 3.6
3 Female 32 23 Left AUS 5  1.9  2.2 3.4
4 Female 65 26 Left AUS 4.6  2.7  1.9 2.8
5 Female 58 30 Left Parathyroid (presumed) 2.5  2.6  3.5 3.5
6 Female 60 25 Right Parathyroid (presumed) 0.1  0.8  0.6 0.8
7 Female 52 40 Left Hurthle cell neoplasm 6.3  2.6  3 3.8
8 Female 17 20 Left Adenomatoid nodule 5.4  2.2  2.6 4.3
9 Female 24 23 Right AUS 5.2  2  2.7 4.2
10 Female 49 39 Left Adenomatoid nodule 5.6  1.3 x1.4 1.9
11 Female 37 26 Right SFN 6.8  1.9  2.5 1.7
12 Female 46 32 Left Adenomatoid nodule 5.6  3.3  2.9 4.1
13 Female 32 38 Right PTC 6.1  1.4  2.3 1.5
14 Female 44 22 Right Adenomatoid nodule 5.3  2  2.8 4

AUS = Atypia of Undetermined Significance.

BMI = Body Mass Index.
NA = Not Available.

Table 2
Summary of intraoperative events and postoperative complications .

Case Method Surgery Total operative Specimen Specimen size Final Inadvertent removal of Complications
time (min) divided (cm) pathology parathyroid
1 Robotic Lobectomy 322 Yes 6.5  4  1.8 Benign No None
2 Robotic Lobectomy 287 Yes 6.5  3.2  2 Benign No None
3 Robotic Lobectomy 377 Yes 5  3  1.5 Benign No Temporary lip
numbness
4 Robotic Lobectomy, 290 No 4.6  2.6  1.2 Benign No None
parathyroidectomy
5 Endoscopic Parathyroidectomy 336 No 3.5  2.5  1 Parathyroid No None
6 Endoscopic Parathyroidectomy 232 No 1.5  0.8  0.3 Parathyroid No None
7 Endoscopic Lobectomy 343 No 4.5  2.7  1 Benign No Temporary vocal
fold palsy
8 Endoscopic Lobectomy 238 No 4.2  2.5  1.8 Benign No None
9 Endoscopic Lobectomy 208 No 5.3  3.2  1.9 Benign No None
10 Endoscopic Lobectomy 282 No 5.1  2.1  1 Benign Yes: Intrathyroidal None
11 Endoscopic Lobectomy 213 No 0.8  2.6  1.5 Benign No None
12 Robotic Lobectomy 448 No 4.4  2.9  2.0 Benign No None
13 Robotic Lobectomy 366 No 5.1  3  2.1 1.3 cm PTC No None
14 Endoscopic Lobectomy 189 No 5.2  3.1  1.1 Benign No None

PTC = Papillary Thyroid Cancer.

dissection, midline access to both central neck compartments, permanent recurrent laryngeal nerve injury in 13% in a cohort of
and the ability to offer safe same-day discharge with minimal 8 patients [31]. Modifications led to a vestibular incision
discomfort. [19,32,33], and Anuwong reported excellent outcomes in a series
The evolution of the present technique began with a sublingual of 60 patients [20], as did Yang et al. [21]. Of the 14 cases in our
transoral endoscopic thyroid surgery on pigs and human cadavers series, one (7.1%) each developed symptomatic temporary RLN
[23–30]. Early reports noted a conversion rate of 38% and and temporary lip weakness. Patients had complete resolution of
 J.O. Russell et al. / Oral Oncology 71 (2017) 75–80 79

Table 3
Dermatology life quality index scores.

Case no. DLQI 1 Effect Days postop DLQI 2 Effect Days postop
1 3 Small 20 NA NA NA
2 1 None 30 0 None 171
3 3 Small 19 NA NA NA
4 14 Very large 12 4 Small 98
5 7 Moderate 15 0 None 89
6 10 Moderate 13 NA NA NA
7 1 None 81 0 None 126
8 18 Very large 5 3 Small 26
9 3 Small 13 NA NA NA
10 6 Moderate 17 NA NA NA
11 4 Small 7 0 None 49
12 17 Very large 8 NA NA NA
13 5 Small 12 NA NA NA
14 0 None 10 NA NA NA

DLQI = Dermatology of Life Quality Index.

NA = Not Available.

these problems within 3 months (RLN) and 1 month (lip) of sur- a learning curve exists for remote-access thyroidectomy, requiring
gery. Other remote access approaches have been associated with between 20 and 50 cases [14,21,37]. In a series of 60 patients using
serious complications [13,34,35]. All of those approaches also a transoral endoscopic technique to the thyroid gland, comparable
require cutaneous incisions. surgical times are reported to the standard open transcervical
Quality of life studies have demonstrated that a cervical incision approach [20]. Transoral thyroid surgery may best be provided
can have negative consequences. Choi et al. used the DLQI to inves- by high volume thyroid surgeons who are well situated to develop
tigate the impact of thyroid scars on the quality of life and found and perfect these techniques. It is notable, however, that despite
the mean score to be 9.02, similar to that of patients who suffer the prolonged operative times during the initial learning curve,
from chronic skin disease such as psoriasis, vitiligo and severe ato- there were no permanent complications.
pic dermatitis. Furthermore, they found that quality of life was not There are numerous advantages to the transoral vestibular
associated with the severity of the scar, but rather with the pres- approach. First, the natural orifice incisions are completely incon-
ence of the scar itself [4]. Using the same instrument, the DLQI spicuous. Second, the approach allows excellent visualization of
median score of 3 for a transoral vestibular approach in this series the bilateral recurrent laryngeal nerves (RLN) near their insertion
was much better than traditional cervical incisions. We expect that into the larynx. Third, the distal identification of the RLN at its
scores will continue to improve for each patient as time passes, as insertion is familiar to most experienced endocrine surgeons, and
the surveys were administered very early in the postoperative per- provides a favorable angle of dissection along the plane of the
iod for most patients. nerve. Fourth, the additional soft tissue dissection needed to
Appropriate patient selection is critical to the success of the approach the thyroid through this approach is relatively limited,
transoral vestibular approach. Patients may have a history of keloid which may lend itself to application in patients with a higher
or hypertrophic scar formation and/or be strongly motivated to BMI. Finally, critical structures such as the esophagus and carotid
avoid a cervical incision [5]. Patients should be screened for con- arteries do not need to be exposed in the field of dissection.
traindications that affect patient positioning and intraoperative We used a combination of both endoscopic and robotic tech-
dissection during this procedure, such as cervical spine disease, niques. The endoscopic approach affords the surgeon tactile feed-
previous surgery, thyroiditis or irradiation of the neck. We recom- back, provides quicker and more fluid switching of instruments,
mend initiating this procedure in patients with smaller benign or and avoids the time required to dock the robot. In contrast, the
suspicious nodules (<6 cm). This approach does not appear to be robot provides wristed instrumentation, additional arms, and a
limited by body habitus, as the approach was completed success- high-resolution, three dimensional view. These robotic advantages
fully for patients with a BMI as high as 44. Previous attempts to may be best utilized for smaller tumors or malignancies. The da
apply novel remote access approaches in a Western population Vinci robot is not FDA approved for head and neck surgery, and this
with a higher BMI have had complications that served to quell must be disclosed to the patient as an off-label application. A sur-
early enthusiasm [5]. geon’s choice between endoscopic and robotic techniques is ulti-
As with any novel surgical technique, the importance of the sur- mately determined by factors including skill set, access to
gical informed consent process cannot be overstated [36]. Patients facilities, equipment, and cost.
should undergo preoperative imaging, including axial imaging if With any surgery in the central neck, the ability to protect the
there are concerns for substernal extension, and diagnostic tissue recurrent laryngeal nerve is paramount. In this series, we demon-
sampling. In our first attempted transoral approach, the preopera- strate that the RLN can be safely identified and even dissected
tive ultrasound underestimated the size of the thyroid nodule. To via this approach. We also demonstrate that, in some cases of
avoid this problem, we now perform a surgeon-directed ultra- benign nodules, the gland can be safely freed from the trachea near
sound preoperatively on all patients and perform additional axial the midline after freeing lateral attachments and rotating the lobe
imaging when there is concern for substernal extent. medially. In cases where more thorough identification of the nerve
In this series the operative time is noted to be substantially is required, this can be completed as demonstrated repeatedly in
longer than that required to complete a standard open lobectomy this series.
or parathyroidectomy (unpublished data specific to the authors). The 2015 ATA guidelines on management of thyroid nodules
As with any novel surgical technique there is a learning curve. suggest that a diagnostic lobectomy for cytologically indetermi-
We did note a trend towards shorter operative times with succes- nate nodules 4 cm or smaller in the appropriate clinical context
sive cases, highlighted by the fact that the first case took 322 min may be sufficient therapeutic treatment if these nodules are
while the last took 189 min. Other authors have demonstrated that ultimately proven to be differentiated thyroid cancer on final
80 J.O. Russell et al. / Oral Oncology 71 (2017) 75–80

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