Postsurgical Outcomes and Surgical Completeness of Robotic Thyroid Surgery: A Single Surgeon's Experience on 700 Cases

Abstract

Background:

Advanced technology and understanding of robotic surgical system have rendered robotic thyroid surgery more expanding. The aim of this study was to identify the periodic changes in postsurgical outcomes of robotic thyroid surgery performed by a single surgeon.

Methods:

We conducted a retrospective review of 700 robotic thyroid surgery cases using gasless trans-axillary approach.

Results:

All patients underwent successful operations without conversion to open surgery, and were mostly younger than 45 years, female, less-extended thyroid surgery and lymph node dissection, and thyroid cancer. The median follow-up period was 67 months (12–99 months). Regarding technical outcomes, the operation time declined steeply after 100 consecutive cases, and reached 120.0–132.7 minutes for thyroid lobectomy and 162.9–174.1 minutes for total thyroidectomy (TT). The most common complication was transient hypoparathyroidism (43.7%), whose incidence decreased steeply to a range of 9.1% to 25.0% after 300 consecutive cases. Regarding surgical completeness for thyroid cancer, an average of seven lymph nodes was retrieved through central compartment node dissection without fluctuation over time. The proportion of the patients with serum stimulated thyroglobulin levels <10 ng/mL at the time of radioactive iodine remnant ablation after TT and <1 ng/mL 6–12 months after the first remnant ablation ranged between 86.4%–100% and 66.7%–100%, respectively, without significant fluctuation.

Conclusion:

For properly selected patients, robotic thyroid surgery is useful surgical option with reliable technical outcome and surgical completeness and cosmetic benefit.

Introduction

Surgical technology for differentiated thyroid cancer (DTC) has continuously developed following the introduction of endoscopic thyroid surgery. Notably, robotic surgical system has been adopted since the 2000s to eliminate visible neck scar and overcome the limitations of conventional endoscopic thyroid surgery.^1,2 Various remote approaches including gasless trans-axillary approach, bilateral axillo-breast approach, and trans-oral vestibular approach are employed for performing robotic thyroid surgery, each with its own merits and demerits.^2–13

Several meta-analysis studies have compared the postsurgical outcomes of robotic thyroid surgery for DTC to those of conventional open surgery, and reported comparable outcomes in terms of technical safety and surgical completeness.^10,14–18 However, the long-term oncologic outcome of robotic surgery for DTC is difficult to be directly evaluated based on structural recurrence, because postsurgical course of DTC is usually indolent with excellent prognosis and the median follow-up period of patients treated by robotic surgery is yet to reach 10 years.^19,20

The aim of this study is to review the postsurgical outcomes of 700 robotic thyroid surgeries that used gasless trans-axillary approach with double incision, all of which were performed by a single surgeon. We specifically analyzed the technical safety and surgical completeness, and sought to identify any changes over time.

Materials and Methods

Patient population

Medical records of 700 consecutive patients who underwent robotic thyroid surgery as an initial operation at Asan Medical Center (Seoul, Korea) between December 2008 and January 2017 were retrospectively reviewed. The study protocol was approved by our institutional review board, and the requirement for informed consent from each patient was waived due to the non-interventional nature of the study.

We investigated the baseline clinicopathologic features of the patients, including the parameters associated with technical outcomes and surgical completeness. The technical outcomes included operation time and perioperative complication rates, and the surgical completeness was assessed by the number of retrieved lymph nodes and serum stimulated thyroglobulin (sTg) levels at the time of radioactive iodine (RAI) remnant ablation (ablation sTg) and 6–12 months after remnant ablation (control sTg) following total thyroidectomy (TT). These postsurgical outcomes were divided and compared by 100 consecutive cases.

Preoperative diagnosis and staging work up

The preoperative diagnosis was determined by ultrasonography-guided fine-needle aspiration cytology (FNAC) or core needle biopsy (CNB). In the cases of preoperative diagnosis of papillary thyroid carcinoma (PTC), preoperative staging work-up using neck ultrasonography and computed tomography was performed to evaluate tumor characteristics and cervical lymph node status. Conversely, for patients with preoperative diagnosis of follicular or Hürthle cell neoplasm, a diagnostic thyroid lobectomy was carried out without any preoperative staging work-up.

Inclusion and exclusion criteria for robotic thyroid surgery

Before 2014, we used the following inclusion criteria: (1) follicular or Hürthle cell neoplasm with a primary tumor size not exceeding 4 cm, (2) PTC with a size ≤2 cm in maximum diameter, and (3) minimal invasion to the anterior thyroid capsule and strap muscle. Since 2014, the inclusion criteria were extended and now we only apply strict exclusion criteria: (1) definite posterior capsular invasion especially adjacent to the tracheoesophageal groove, (2) lateral lymph node metastasis, and (3) distant metastasis at presentation. All patients were informed about both robotic and conventional open surgery, and the decision of surgical option was based on the patient's preference.

Surgical strategy in patients with thyroid cancer

Before 2016, TT was recommended for almost all patients with primary tumors >1 cm, which was based on the earlier American Thyroid Association (ATA) guidelines. Since 2016, however, the surgical paradigm was shifted to more conservative surgery based on the revised ATA guidelines, and therefore TT was recommended only for patients with primary tumors >4 cm, bilateral cancers, gross extrathyroidal extension (T4 classification), and lateral lymph node metastasis found during preoperative evaluation or operation.

At our institution, central compartment node dissection (CCND) is routinely performed for patients with thyroid cancer; at minimum, unilateral prophylactic CCND is performed even in cases with absence of suspicious lymph nodes on preoperative imaging studies or during surgery. Bilateral CCND is performed on patients with suspicious lymph nodes or lymph node enlargement in the contralateral central compartment, or in those with bilateral cancer. Compartment-based nodal dissection is performed in preference. All surgeries included in this study were performed by a single endocrine surgeon (J.H.Y.).

RAI remnant ablation protocol

Subsequent RAI remnant ablation was performed 4–6 weeks after the initial operation, according to the protocol established by the Endocrinology Division of Asan Medical Center.²¹ At the time of remnant ablation, following thyroid hormone withdrawal or recombinant human thyroid stimulating hormone (rh-TSH) administration, the ablation sTg level (reference range, 1.0–23.3 ng/mL) was measured with the anti-Tg antibody level (reference range <60 U/mL) when the TSH level (reference range, 0.4–5.0 mU/L) was >30 mU/L. A postablation whole-body scan (WBS) was performed 5–7 days after the administration of iodine-131.

Postoperative follow-up protocol

All patients received follow-up examinations at the outpatient clinic. Patients who underwent thyroid lobectomy alone or TT without RAI remnant ablation were followed up at 1, 6, and 12 months, and annually thereafter with TSH suppression therapy. Thyroid function tests were routinely performed at every visit, and neck ultrasonography was performed once per year.

In patients who underwent TT with RAI remnant ablation, diagnostic WBS following thyroid hormone withdrawal or rh-TSH administration was performed 6–12 months after remnant ablation with the simultaneous measurement of control sTg. Serum Tg/anti-Tg antibody measurement and neck ultrasonography were performed on all patients during the follow-up period. When the control sTg was ≥1 ng/mL and neck ultrasonography showed no evidence of disease,¹⁷ F-deoxyglucose positron emission tomography or chest computed tomography were considered to localize persistent or remnant disease. Any patients suspected to have loco-regional recurrence underwent ultrasonography-guided FNAC or CNB.

Structural recurrence was defined as the appearance of cytologically- or histopathologically proven malignant tissue, or the appearance of highly suspicious structural lesions on cross-sectional or functional imaging studies after a period of no evidence of disease for at a minimum of 1 year after the initial treatment. However, unlike extra-cervical structural lesion (distant metastasis), even highly suspicious loco-regional structural lesion on cross-sectional or functional imaging studies was not considered as a structural recurrence until the lesion was confirmed by FNAC or surgical biopsy.

Lesions not confirmed cytologically or histopathologically were reevaluated by serial ultrasonography and repeated FNAC or surgical biopsy. Structural persistent disease was defined as the appearance of structural lesions without a period of no evidence of disease for 1 year after the initial treatment. Biochemical recurrence, which is characterized by an elevated serum Tg level without clinical evidence of structural disease, was not classified as true recurrence.

Statistical analysis

Categorical variables are presented as numbers and percentages, and continuous variables are presented as means ± standard deviations or medians with ranges. Comparisons of characteristics between groups were performed using the t test for continuous variables and Fisher's exact test for categorical variables. All P values were two-sided. Data were considered statistically significant at P values < .05. All statistical analyses were performed using the SPSS software version 18.0 (IBM SPSS).

Results

Baseline clinicopathological features

Baseline clinicopathological features of patients who received gasless trans-axillary robotic thyroid surgery are shown in Table 1, demonstrating predominance of young age (<45 years old), female, less-extended surgery, involving a thyroid lobectomy and ipsilateral CCND, and thyroid cancer. The mean operative times for thyroid lobectomy and TT were 127.3 and 176.7 minutes, respectively (Table 1).

Table 1.

Baseline Clinicopathologic Features of Patients Who Underwent Robotic Thyroid Surgery

Variables	n = 700
Age, year (range)	39.9 ± 9.3 (15–61)
Sex, n (%)
Male	56 (8.0)
Female	644 (92.0)
Pathology, n (%)
Benign	25 (3.6)
Malignant	675 (96.4)
Extent of thyroid surgery, n (%)
Thyroid lobectomy	510 (72.9)
TT	190 (27.1)
Extent of LN dissection, n (%)
None	31 (4.4)
Ipsilateral CCND	634 (90.6)
Bilateral CCND	35 (5.0)
Operation time, minutes (range)
Thyroid lobectomy	127.3 ± 27.0 (60.0–255.0)
TT	176.7 ± 34.5 (107.0–297.0)
Postoperative hospital stay, day (range)	3.3 ± 1.3 (2–18)

CCND, central compartment node dissection; TT, total thyroidectomy.

Clinicopathologic findings in patients treated with robotic surgery for thyroid cancer

Clinicopathologic findings of the patients who were treated with robotic surgery for thyroid cancer are shown in Table 2. PTC was the most common thyroid malignancy (98.5%) treated with robotic thyroid surgery. Extrathyroidal extension and lymph node metastasis were observed in 49.0% and 38.9% of the patients, respectively. The mean number of retrieved lymph nodes was seven for ipsilateral CCND and nine for bilateral CCND.

Table 2.

Clinicopathologic Findings in Patients Treated with Robotic Thyroid Surgery for Differentiated Thyroid Cancer

Characteristics	n = 675
Histopathology, n (%)
Papillary carcinoma	665 (98.5)
Follicular carcinoma, minimally invasive	9 (1.3)
Medullary carcinoma	1 (0.2)
Extent of thyroid surgery, n (%)
Thyroid lobectomy	510 (72.9)
TT	190 (27.1)
Extent of lymph node dissection, n (%)
None	31 (4.4)
Ipsilateral CCND	634 (90.6)
Bilateral CCND	35 (5.0)
Primary tumor size, cm (range)	0.9 ± 0.6 (0.1–5.0)
Extrathyroidal extension, n (%)	330 (49.0)
Multiplicity, n (%)	145 (21.5)
Bilaterality, n (%)^a	61 (9.1)
Lymph node metastasis, n (%)	269 (38.9)
Retrieved central lymph node, n (range)
Ipsilateral CCND	7.0 ± 4.5 (0–32)
Bilateral CCND	9.1 ± 5.4 (1–22)
Structural recurrence, n (%)	6 (0.8)

Bilaterality was evaluated only in TT.

CCND, Central compartment node dissection; TT, total thyroidectomy.

Six patients (0.8%) had structural recurrence during follow-up period. Among those, 4 recurrences occurred in lateral lymph node after TT and 2 in remaining thyroid gland after initial thyroid lobectomy. The median follow-up period was 67 months (range, 7–103).

Changes in various technical outcomes following robotic thyroid surgery

The technical outcomes were assessed with regard to the operation time and the rate of perioperative complications, and grouped by 100 consecutive cases (Table 3).

Table 3.

Changes in Technical Outcomes of Robotic Thyroid Surgery Grouped by 100 Consecutive Cases

Complications	Total	1–100	101–200	201–300	301–400	401–500	501–600	601–700	P
Operation time, minutes (mean ± SD)
Less than total	127.3 ± 27.0	141.9 ± 26.3	127.3 ± 24.0	132.7 ± 26.8	125.6 ± 28.7	123.3 ± 21.9	120.0 ± 29.6	123.0 ± 24.3	<.001
Total	176.7 ± 34.5	192.5 ± 35.7	169.3 ± 28.2	191.7 ± 39.8	169.9 ± 35.7	174.1 ± 23.4	162.9 ± 37.0	171.4 ± 34.8	.012
Transient hypoparathyroidism, n (%)^*	83/190 (43.7)	15/23 (65.2)	32/53 (60.4)	20/35 (57.1)	8/32 (25.0)	4/22 (18.2)	1/11 (9.1)	3/14 (21.4)	<.001
Permanent hypoparathyroidism, n (%)^*	2/190 (1.1)	0/23	0/53	1/35 (2.8)	1/32 (3.0)	0/22	0/11	0/14	.130
RLN injury, n (%)	6 (0.9)	1 (1.0)	2 (2.0)	0	1 (1.0)	1 (1.0)	1 (1.0)	0	.247
Seroma, n (%)	7 (0.9)	2 (2.0)	1 (1.0)	1 (1.0)	0	1 (1.0)	0	1 (1.0)	.668
Hematoma, n (%)	1 (0.1)	0	0	0	1 (1.0)	0	0	0	.422
Chyle leakage, n (%)	1 (0.1)	0	1(1.0)	0	0	0	0	0	.422
Infection, n (%)	6 (0.9)	3 (3.0)	0	0	1 (1.0)	1 (1.0)	0	1	.104
Tracheal injury, n (%)	4 (0.6)	1 (1.0)	2 (2.0)	0	0	0	1 (1.0)	0	.364
Esophageal injury, n (%)	0	0	0	0	0	0	0	0
Brachial plexus neuropathy, n (%)	0	0	0	0	0	0	0	0

The number was divided by TT cases in each period because transient hypocalcemia and permanent hypocalcemia were evaluated only in TT patients.

SD, standard deviation; TT, total thyroidectomy.

The operation times for both thyroid lobectomy and TT steeply decreased after a total of 100 consecutive cases, and reached a plateau. The most common complication related to robotic thyroid surgery was transient hypoparathyroidism following TT (43.7%). However, the incidence of transient hypoparathyroidism steeply decreased after a total of 300 consecutive cases, and was maintained at a rate ranging from 9.1% to 25.0%. Permanent hypoparathyroidism and intraoperative recurrent laryngeal nerve injury was observed in 1.1% and 0.9% of the patients, respectively. The rates of surgery-related complications, except for transient hypoparathyroidism, did not show significant changes over time.

Changes in surgical completeness following robotic thyroid surgery

The surgical completeness of robotic surgery in patients who underwent robotic surgery for thyroid cancer was evaluated with regard to the number of retrieved lymph nodes and ablation/control sTg levels, and grouped by 100 consecutive cases (Table 4).

Table 4.

Changes in Surgical Completeness of Robotic Thyroid Cancer Surgery Grouped by 100 Consecutive Cases

Characteristics	Total	1–100	101–200	201–300	301–400	401–500	501–600	601–700	P
Pathology, n (%)
Benign	25	2	0	1	7	3	4	8	.018
Malignant	675	98	100	99	93	97	96	92	.005
Retrieved LNs (mean ± SD)	7.1 ± 4.6	6.3 ± 4.0	6.9 ± 4.9	6.7 ± 4.9	6.5 ± 4.0	7.7 ± 4.6	4.5 ± 4.5	8.3 ± 4.9	.028
Extent of thyroid surgery, n (%)^a
Less than total	488 (72.3)	76	47	64	63	75	85	78	<.001
Total	187 (27.7)	22	53	35	30	22	11	14	<.001
RAI Tx, n (%)	157/190 (82.6)	20/22 (90.9)	49/53 (92.5)	31/35 (88.6)	23/30 (76.7)	17/22 (77.3)	6/11 (54.5)	11/14 (78.6)	.036
Anti-Tg Ab (+), n (%)	43/157 (22.6)	5/20 (25.0)	13/49 (26.5)	9/31 (29.0)	4/23 (17.4)	5/17 (29.4)	3/6 (50.0)	4/11 (36.4)	.771
Ablation sTg, <10 ng/mL, n (%)	106/114 (93.0)	15/15 (100)	33/36 (91.7)	19/22 (86.4)	17/19 (89.5)	12/12 (100)	3/3 (100)	7/7 (100)	.583
Control sTg, <1 ng/mL, n (%)	109/112 (97.3)	15/15 (100)	34/35 (97.1)	20/21 (95.2)	19/19 (100)	12/12 (100)	2/3 (66.7)	7/7 (100)	.239

The extent of thyroid surgery is counted in case of malignancy.

Ablation sTg, serum thyroglobulin measured at the time of remnant ablation after thyroid hormone withdrawal; anti-Tg Ab, anti-thyroglobulin antibody; control sTg, serum thyroglobulin measured 6–12 months after remnant ablation at the time of diagnostic whole body scan after thyroid hormone withdrawal or thyrogen administration.

LN, lymph node; RAI Tx, radioactive iodine treatment; RLN, recurrent laryngeal nerve; SD, standard deviation; UD, undetectable serum thyroglobulin value defined as below functional sensitivity (0.2 ng/mL in this report).

The mean number of retrieved lymph nodes was seven, which was maintained without significant fluctuation over time. A total of 190 patients received TT, and among those, 157 patients joined RAI remnant ablation. After excluding the patients with positive anti-Tg Ab levels, 114 and 112 patients were evaluated with regard to ablation and control sTg levels, respectively. The proportion of the patients with ablation sTg <10 ng/mL and control sTg level <1 ng/mL was 93.0% (range, 91.7%–100%) and 97.3% (range, 66.7%–100%), respectively, which did not show significant periodic changes.

Discussion

In this study, we identified the changes in clinicopathologic features and postsurgical outcomes of robotic thyroid surgery based on a single surgeon's experience of 700 cases. Robotic thyroid surgery was preferred by young female patients who may have been more interested in the cosmetic benefit of robotic surgery.^22,23 Most of the patients had PTCs, and received less extended surgery. This trend of less extended surgery was more prominent in cases after 2016, when the revised ATA guideline was released. Most technical and short-term oncological parameters did not show significant changes during the study period. Only parameters that showed changes over time were operation time and incidence of transient hypoparathyroidism, which declined after 100 and 300 consecutive cases, respectively.

Many previously published meta-analysis studies have reported comparable or superior outcomes of robotic thyroid surgery to conventional open surgery, with respect to technical safety, surgical completeness, and quality of life.^{10,14–18,24} The oncological safety of robotic thyroid surgery has been evaluated with respect to the number of retrieved lymph nodes and surgical completeness based on the postoperative serum Tg level and the proportion of sTg <1 ng/mL after the first ablation following TT and RAI remnant ablation; this is because the follow-up period of robotic surgery is yet too short to directly evaluate its oncological outcome with regard to structural recurrence.

While several studies have demonstrated that robotic surgery was associated with smaller number of retrieved lymph nodes and higher postoperative serum Tg levels following TT and RAI remnant ablation than open surgery, others reported no significant difference between the two groups regarding the same parameters.^{1,4–6,9,19,20,25–28} These discrepancies have been shown to be due to the confusion whether the serum Tg levels measured were suppressed or stimulated, and the simple sum of retrieved lymph nodes not divided into central and lateral ones.

Excluding the studies that did not mention whether serum Tg was stimulated or not, the pooled data comparing the sTg levels did not show significant difference between robotic surgery and open surgery groups. Furthermore, in subgroup analysis according to the type of lymph node dissection (CCND or lateral lymph node dissection), the number of retrieved lymph nodes was reported as not significantly different between the two groups.^{1,4,5,19,20,25–28} Additionally, the proportion of sTg <1 ng/mL after the first ablation was comparable to that of open surgery, ranging from 64.7% to 64.8%.

In this study, an average of seven lymph nodes were harvested through CCND without significant changes over time; also, the proportion of sTg <1 ng/mL after the first ablation ranged from 66.7% to 100%, which was higher than that reported from previous studies, and did not show significant fluctuation during the study period.

The technical safety was evaluated with regard to the operation time and the perioperative complication rate. The operation time of robotic surgery using gasless trans-axillary approach was reported to be significantly longer than open surgery, ranging from 128.6 to 277.4 minutes for TT and from 99.3 to 133.5 minutes for thyroid lobectomy. The major complication rates of robotic surgery were reported to be comparable to those of open surgery as follows: transient hypoparathyroidism, 6.3%–48.2%; permanent hypoparathyroidism, 0%–4.8%; permanent recurrent laryngeal nerve palsy, 0%–1.6%; and postoperative bleeding, 0%–2.3%.

The overall operation time and overall major complication rates in this study were within the range of those rates reported from previous studies.^{1,4–6,9,20,25–28} However, their changes over time and required number of cases for a significant decline were noteworthy. While the operation time for both TT and thyroid lobectomy steeply decreased after 100 consecutive robotic surgeries, the incidence of transient hypoparathyroidism continued to be high until 300 consecutive cases were performed. This may be due to the difference of surgical proficiency required for shortening the operation time itself and lowering the incidence of transient hypoparathyroidism.

The longer operation time of robotic thyroid surgery than open surgery is mainly due to the additional time required for creating working space and robotic docking. Therefore, the operation time itself can be shortened by reducing this additional time through accumulation of experience. However, lowering the incidence of transient hypoparathyroidism requires a more complex surgical proficiency, including advanced anatomical understanding of feeding vessels to and venous drainage from parathyroid glands, meticulous dissection, individual ligation, and appropriate handling of energy device ensuring the safe distance to avoid thermal injury to parathyroid glands.

This study has a retrospective observational design, and not a comparative one with conventional open surgery group, which is an obvious inherent limitation. Nevertheless, this study is valuable in that it focused on identifying the changes of clinicopathologic features and postsurgical outcomes of robotic thyroid surgery by a single surgeon over time, and had a larger scale of patient cohort with longer follow-up period than previous studies.

In conclusion, robotic thyroid surgery using gasless trans-axillary approach appears to be a feasible surgical option with sufficient technical safety and surgical completeness in addition to cosmetic benefits for properly selected thyroid cancer patients, as mentioned earlier in the inclusion and exclusion criteria.

Footnotes

Disclosure Statement

No competing financial interests exist.

References

Kang

, Jeong

, Yun

, et al. Robot-assisted endoscopic surgery for thyroid cancer: Experience with the first 100 patients. Surg Endosc, 2009; 23:2399–2406.

Kang

, Lee

, et al. Robotic thyroid surgery using a gasless, transaxillary approach and the da Vinci S system: The operative outcomes of 338 consecutive patients. Surgery, 2009; 146:1048–1055

Kim

, Chai

, Dionigi

, Anuwong

, Richmon

. Transoral robotic thyroidectomy: Lessons learned from an initial consecutive series of 24 patients. Surg Endosc, 2017 [Epub ahead of print]; DOI: 10.1007/s00464-017-5724-5.

Kim

, Kim

, Hur

, et al. Is robotic surgery superior to endoscopic and open surgeries in thyroid cancer?. World J Surg, 2011; 35:779–784.

Lee

, Lee

, Nah

, Soh

, Chung

. Comparison of endoscopic and robotic thyroidectomy. Ann Surg Oncol, 2011; 18:1439–1446.

Lee

, Ryu

, Park

, et al.: Early surgical outcomes comparison between robotic and conventional open thyroid surgery for papillary thyroid microcarcinoma. Surgery, 2012; 151:724–730.

Lee

, Yi

, Sung

, Chung

, Yoon

, Hong

. Surgical outcomes of robotic thyroid surgery using a double incision gasless transaxillary approach: Analysis of 400 cases treated by the same surgeon. Head Neck, 2014; 36:1413–1419.

Richmon

, Kim

. Transoral robotic thyroidectomy (TORT): Procedures and outcomes. Gland Surg, 2017; 6:285–289.

Tae

, Ji

, Cho

, Lee

, Kim

. Early surgical outcomes of robotic thyroidectomy by a gasless unilateral axillo-breast or axillary approach for papillary thyroid carcinoma: 2 years' experience. Head Neck, 2012; 34:617–625.

10.

Kandil

, Hammad

, Walvekar

, et al. Robotic thyroidectomy versus nonrobotic approaches: A meta-analysis examining surgical outcomes. Surgical Innov, 2016; 23:317–325.

11.

Kang

, Lee

, Ryu

, et al. Initial experience with robot-assisted modified radical neck dissection for the management of thyroid carcinoma with lateral neck node metastasis. Surgery, 2010; 148:1214–1221.

12.

Lee

, Rao

, Youn

. Endoscopic thyroidectomy with the da Vinci robot system using the bilateral axillary breast approach (BABA) technique: Our initial experience. Surg Laparosc Endosc Percutan Tech, 2009; 19:e71–e75.

13.

Lee

, Koo do

, Kim

, et al. Outcomes of 109 patients with papillary thyroid carcinoma who underwent robotic total thyroidectomy with central node dissection via the bilateral axillo-breast approach. Surgery, 2010; 148:1207–1213.

14.

Lang

, Wong

, Tsang

, Wong

, Wan

. A systematic review and meta-analysis comparing surgically-related complications between robotic-assisted thyroidectomy and conventional open thyroidectomy. Ann Surg Oncol, 2014; 21:850–861.

15.

Pan

, Zhou

, Zhao

, et al. Robotic thyroidectomy versus conventional open thyroidectomy for thyroid cancer: A systematic review and meta-analysis. Surg Endosc, 2017; 31:3985–4001.

16.

Jackson

, Yao

, Tufano

, Kandil

. Safety of robotic thyroidectomy approaches: Meta-analysis and systematic review. Head Neck, 2014; 36:137–143.

17.

Son

, Kim

, Bae

, Lee

. Surgical safety and oncologic effectiveness in robotic versus conventional open thyroidectomy in thyroid cancer: A systematic review and meta-analysis. Ann Surg Oncol, 2015; 22:3022–3032.

18.

Wang

, Liu

, Xiong

, Zhu

. Robotic thyroidectomy versus conventional open thyroidectomy for differentiated thyroid cancer: Meta-analysis. J Laryngol Otol, 2015; 129:558–567.

19.

Lee

, Lee

, Kim

, et al. Long-term oncologic outcome of robotic versus open total thyroidectomy in PTC: A case-matched retrospective study. Surg Endosc, 2016; 30:3474–3479.

20.

Tae

, Song

, Ji

, Sung

, Jeong

, Kim

. Oncologic outcomes of robotic thyroidectomy: 5-year experience with propensity score matching. Surg Endosc, 2016; 30:4785–4792.

21.

Kim

, Kim

, et al. Effects of different doses of radioactive iodine for remnant ablation on successful ablation and on long-term recurrences in patients with differentiated thyroid carcinoma. Nucl Med Commun, 2011; 32:954–959.

22.

Bae

, Cho

, Sung

, et al. The current status of endoscopic thyroidectomy in Korea. Surg Laparosc Endosc Percutan Tech, 2008; 18:231–235.

23.

Park

, Chung

, Chang

. Minimally invasive open thyroidectomy. Surg Today, 2001; 31:665–669.

24.

Tae

, Kim

, Yun

, et al. Functional voice and swallowing outcomes after robotic thyroidectomy by a gasless unilateral axillo-breast approach: Comparison with open thyroidectomy. Surg Endosc, 2012; 26:1871–1877.

25.

Lee

, Ryu

, Park

, et al. Excellence in robotic thyroid surgery: A comparative study of robot-assisted versus conventional endoscopic thyroidectomy in papillary thyroid microcarcinoma patients. Ann Surg, 2011; 253:1060–1066.

26.

Tae

, Ji

, Jeong

, Kim

, Choi

, Ahn

. Comparative study of robotic versus endoscopic thyroidectomy by a gasless unilateral axillo-breast or axillary approach. Head Neck, 2013; 35:477–484.

27.

Tae

, Song

, Ji

, Kim

, Choi

. Comparison of surgical completeness between robotic total thyroidectomy versus open thyroidectomy. Laryngoscope, 2014; 124:1042–1047.

28.

, Yoon

, Lee

, et al. Technical and oncologic safety of robotic thyroid surgery. Ann Surg Oncol, 2013; 20:1927–1933.