Hostname: page-component-745bb68f8f-s22k5 Total loading time: 0 Render date: 2025-02-06T07:36:16.884Z Has data issue: false hasContentIssue false

Robotic thyroidectomy versus conventional open thyroidectomy for differentiated thyroid cancer: meta-analysis

Published online by Cambridge University Press:  25 May 2015

Y-C Wang
Affiliation:
Department of Thyroid and Breast Surgery, West China Hospital, Sichuan University, Chengdu, China
K Liu
Affiliation:
Department of Cardiology, West China Hospital, Sichuan University, Chengdu, China
J-J Xiong
Affiliation:
Department of Pancreatic Surgery, West China Hospital, Sichuan University, Chengdu, China
J-Q Zhu*
Affiliation:
Department of Thyroid and Breast Surgery, West China Hospital, Sichuan University, Chengdu, China
*
Address for correspondence: Dr Jingqiang Zhu, Department of Thyroid and Breast Surgery, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China Fax: +86-28-85423822 E-mail: jingqiangzhu@163.com
Rights & Permissions [Opens in a new window]

Abstract

Objective:

To conduct a meta-analysis to compare the short-term outcomes of robotic thyroidectomy and conventional open thyroidectomy for differentiated thyroid cancer.

Methods:

Medline, Embase, Science Citation Index Expanded and the Cochrane Library databases were searched for relevant literature. The evaluated endpoints were intra-operative and post-operative outcomes.

Results:

Twelve eligible, non-randomised comparative studies involving 2513 patients were included, with 923 patients in the robotic thyroidectomy group and 1590 patients in the conventional open thyroidectomy group. Meta-analysis results revealed that robotic thyroidectomy was associated with significantly longer operative time and a lower number of retrieved central lymph nodes, as compared with conventional open thyroidectomy. No significant differences were found between robotic thyroidectomy and conventional open thyroidectomy in terms of post-operative outcomes.

Conclusion:

Robotic thyroidectomy appears to be a feasible and safe surgical procedure for patients with differentiated thyroid cancer. However, more high-quality randomised clinical trials should be undertaken to confirm these findings.

Type
Main Articles
Copyright
Copyright © JLO (1984) Limited 2015 

Introduction

Differentiated thyroid carcinoma is a common malignancy of the thyroid; it is prevalent worldwide but is more common in women.Reference Yang, Gu, Wang, Xiang and Chen1, Reference Davies and Welch2 Conventional open thyroidectomy is an effective cure for thyroid cancer; however, it leaves a long conspicuous scar on the anterior of the neck.Reference Jeryong, Jinsun, Hyegyong, Eilsung, Jiyoung and Insang3 Recent developments in endoscopic thyroidectomy have improved the aesthetic outcome, as no scar is left on the neck.Reference Bae, Cho, Sung, Oh, Jung and Lee4, Reference Kang, Jeong, Yun, Sung, Lee and Lee5 However, endoscopic thyroidectomy is associated with limitations, including a narrow working space on the neck, two-dimensional operative visualisation and inadequate endoscopic instrumentation.Reference Fan and Jiang6Reference Ikeda, Takami, Sasaki, Takayama, Niimi and Kan8 Robotic thyroidectomy performed using the da Vinci® S surgical robotic system overcomes these limitations by providing hand-tremor filtration technology, a three-dimensional operative view, and multi-articulated and fine instrumentation.Reference Fan and Jiang6, Reference Lee, Rao and Youn9, Reference Kandil, Noureldine, Yao and Slakey10

Recently, a few studies have reported the applicability of robotic thyroidectomy for thyroid cancer.Reference Tae, Ji, Jeong, Lee, Jeong and Park7, Reference Kang, Lee, Lee, Lee, Jeong and Lee11, Reference Lee, Kim, Koo do, Choi, Kim and Youn12 However, the general application of robotic thyroidectomy for malignant thyroid tumours continues to be debated.Reference Kang, Jeong, Yun, Sung, Lee and Lee13, Reference Lee, Lee, Lee, Park, Kim and Son14 This is partly because of the small sample size of the studies conducted, which assessed patients within a single institution, and a lack of definitive evidence about recurrence and survival rates.

To date, three published meta-analyses have reported on the feasibility and safety of robotic thyroidectomy compared to that of conventional open thyroidectomy.Reference Lang, Wong, Tsang, Wong and Wan15Reference Sun, Peress and Pynnonen17 However, these meta-analyses included patients with benign and malignant thyroid diseases. No meta-analysis has systematically reviewed the differences between robotic thyroidectomy and conventional open thyroidectomy for differentiated thyroid cancer patients only. Furthermore, since those meta-analysis studies were published, several new studies with greater numbers of participants have been published.Reference Lee, Lee, Lee, Park, Kim and Son14, Reference Kim, Kang, Kang and Park18Reference Noureldine, Jackson, Tufano and Kandil20 Thus, a systematic and comprehensive analysis of the published data on robotic thyroidectomy and conventional open thyroidectomy for differentiated thyroid cancer was undertaken to compare the peri-operative outcomes.

Materials and methods

Systematic literature search

In order to compare robotic thyroidectomy with conventional open thyroidectomy for differentiated thyroid cancer, the databases Medline, Embase, Science Citation Index Expanded and the Cochrane Central Register of Controlled Trials in the Cochrane Library were systematically searched for relevant articles published between January 2003 and May 2014. The following Medical Subject Headings and key words (and the combinations of these headings) were used: ‘robotics’, ‘da Vinci surgical system’, ‘robotic assisted thyroidectomy’, ‘robotic thyroidectomy’, ‘conventional thyroidectomy’, ‘open thyroidectomy’, ‘thyroid neoplasms’ and ‘differentiated thyroid cancer’. Only human studies published in English language with full text descriptions were considered for inclusion. Reference lists from retrieved articles were also examined to identify further relevant studies. The final inclusion of articles was determined by consensus from two reviewers; when this failed, a third author adjudicated.

Inclusion criteria

All included studies fulfilled the following criteria: (1) they compared the outcomes of robotic thyroidectomy with those of conventional open thyroidectomy in differentiated thyroid cancer patients; (2) they clearly documented the operative techniques as ‘robotic’ or ‘conventional open’; and (3) they reported at least one of the outcomes mentioned below. When similar studies were published by the same institution or authors, either the one of higher quality or the most recent publication was included in the analysis.

Exclusion criteria

The following publications were excluded from the analysis: (1) abstracts, case reports, letters, editorials, expert opinions and reviews; (2) studies with no clearly reported outcomes of interest; (3) studies with no control groups; and (4) studies evaluating patients with benign thyroid lesions.

Outcomes measured

Intra-operative and post-operative outcomes were evaluated to compare robotic thyroidectomy and conventional open thyroidectomy. Intra-operative outcomes included operative time and number of retrieved central lymph nodes. Post-operative outcomes included post-operative hospital stay, transient recurrent laryngeal nerve (RLN) palsy, permanent RLN palsy, transient hypocalcaemia, permanent hypocalcaemia, chyle leakage, post-operative suppressed serum thyroglobulin levels and post-operative thyroid stimulating hormone (TSH)-stimulated serum thyroglobulin levels.

Data extraction and quality assessment

Two researchers independently extracted data using standardised forms. Data extracted from each study included patient characteristics, operative details, and post-operative outcomes. The quality of the studies was assessed using the Newcastle–Ottawa Scale,Reference Stang21 with some modifications. Specifically, three factors were examined: patient selection, comparability of the two groups (robotic thyroidectomy and conventional open thyroidectomy) and assessment of outcome. Studies awarded six or more stars were considered as higher quality.Reference Athanasiou, Al-Ruzzeh, Kumar, Crossman, Amrani and Pepper22

Statistical analysis

The meta-analysis was performed using Review Manager software, version 5.0 (Cochrane Collaboration, Oxford, UK). Categorical variables were analysed in terms of odds ratios and corresponding 95 per cent confidence intervals (CIs). Continuous variables were analysed using weighted mean differences and corresponding 95 per cent CIs. The pooled effect was calculated using either a fixed-effects or random-effects model based on heterogeneity. Heterogeneity was measured using the chi-square test and I2 statistic, with a p value of <0.1 considered significant.Reference Higgins, Thompson, Deeks and Altman23 If the I2 statistic was over 50 per cent, the random-effects analysis was performed. Subgroups were used for the sensitivity analysis. Funnel plots were created to evaluate the potential publication bias.

Results

Study characteristics

The search strategy initially identified 176 potentially relevant clinical studies. Twenty-seven articles were selected for further assessment following application of the study criteria. Of these, five studies were published without comparison,Reference Lee, Kim, Koo do, Choi, Kim and Youn12, Reference Kang, Jeong, Yun, Sung, Lee and Lee13, Reference Lee, Yun, Nam, Choi, Chung and Soh24Reference Son, Park, Lee, Lee, Kim and Kang26 five studies reported benign and malignant tumour cases,Reference Tae, Ji, Jeong, Lee, Jeong and Park7, Reference Kim, Kim, Chang, Yoo and Kim27Reference Landry, Grubbs, Warneke, Ormond, Chua and Lee30 one study only investigated benign tumour cases,Reference Park, Lee, Park, Jeong, Kang and Jeong31 and two studies included other operations;Reference Ji, Song, Bang, Lee, Park and Tae32, Reference Foley, Agcaoglu, Siperstein and Berber33 these studies were excluded from the analysis. In addition, four studies were published by the same institute and had overlapping patient populations;Reference Kim, Kang, Kang and Park18, Reference Kim, Kang and Park34Reference Tae, Ji, Cho, Lee, Kim and Kim36 only the higher quality studiesReference Kim, Kang, Kang and Park18, Reference Tae, Song, Ji, Kim, Kim and Choi35 were included.

A total of 12 studies published between 2010 and 2014 that matched the inclusion criteria were included in this study.Reference Lee, Lee, Lee, Park, Kim and Son14, Reference Kim, Kang, Kang and Park18Reference Noureldine, Jackson, Tufano and Kandil20, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37Reference Lee, Koo do, Im, Park, Choi and Paeng43 All 12 studies were non-randomised, controlled trials. A flow chart demonstrating the process of article selection is shown in Figure 1.

Fig. 1 Flow chart showing the process of article identification and selection.

The general characteristics of studies included in the meta-analysis are summarised in Table I. The quality assessment results for these 12 studies are presented in Table II.

Table I Characteristics of included studies

*1 = age, 2 = gender, 3 = tumour size, 4 = multiplicity, 5 = bilateralism, 6 = type of thyroidectomy, 7 = extrathyroidal extension, 8 = tumour classification, 9 = node classification, 10 = tumour–node–metastasis stage. Pts = patients; SD = standard deviation; RT = robotic thyroidectomy; COT = conventional open thyroidectomy

Table II Quality assessment results*

* Quality was assessed using the Newcastle–Ottawa Scale,Reference Stang21 with some modifications. Comparability variables include age, tumour size, multiplicity, bilateralism, extrathyroidal extension, type of thyroidectomy and tumour–node–metastasis stage. Studies awarded six or more stars were considered higher quality.Reference Athanasiou, Al-Ruzzeh, Kumar, Crossman, Amrani and Pepper22 RT = robotic thyroidectomy; COT = conventional open thyroidectomy

The 12 studies involved 2513 patients: 923 patients in the robotic thyroidectomy group and 1590 patients in the conventional open thyroidectomy group. In terms of surgical approaches, eight studies were performed using a gasless transaxillary approach,Reference Lee, Lee, Lee, Park, Kim and Son14, Reference Lee, Kwon, Bae and Chung19, Reference Noureldine, Jackson, Tufano and Kandil20, Reference Kang, Lee, Park, Jeong, Park and Lee37Reference Lee, Nah, Kim, Ahn, Soh and Chung39, Reference Yi, Yoon, Lee, Sung, Chung and Kim41, Reference Ryu, Lee, Park, Kang, Jeong and Hong42 three studies were performed using a bilateral axillo-breast approach,Reference Kim, Kang, Kang and Park18, Reference Kim, Kim, Hur, Kim, Lee and Choi40, Reference Lee, Koo do, Im, Park, Choi and Paeng43 and one study was performed using a gasless unilateral axillo-breast or axillary approach.Reference Tae, Song, Ji, Kim, Kim and Choi35 One study focused on robotic modified radical neck dissection for papillary thyroid carcinoma with lateral neck metastasis.Reference Lee, Kwon, Bae and Chung19 Two studies reported on patients with papillary thyroid cancer and follicular thyroid cancer.Reference Noureldine, Jackson, Tufano and Kandil20, Reference Lee, Nah, Kim, Ahn, Soh and Chung39 The patients in the other studies had only papillary thyroid cancer. Eleven studies were performed in KoreaReference Lee, Lee, Lee, Park, Kim and Son14, Reference Kim, Kang, Kang and Park18, Reference Lee, Kwon, Bae and Chung19, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37Reference Lee, Koo do, Im, Park, Choi and Paeng43 and one study was carried out in the USA.Reference Noureldine, Jackson, Tufano and Kandil20

Meta-analysis results

The results of the meta-analysis are summarised in Table III.

Table III Meta-analysis results of interest

Pts = patients; OR = odds ratio; WMD = weighted mean difference; CI = confidence interval; post-op = post-operative; RLN = recurrent laryngeal nerve; TSH = thyroid stimulating hormone

Intra-operative outcomes

The operative time was reported in six studies.Reference Lee, Kwon, Bae and Chung19, Reference Noureldine, Jackson, Tufano and Kandil20, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37, Reference Kim, Kim, Hur, Kim, Lee and Choi40, Reference Ryu, Lee, Park, Kang, Jeong and Hong42 The pooled data revealed that the operative time was significantly longer in the robotic thyroidectomy group than the conventional open thyroidectomy group (weighted mean difference = 53.59, 95 per cent CI = 14.67–92.51, p = 0.007), although there was significant heterogeneity between the studies (I2 = 99 per cent) (Figure 2a). The number of retrieved central lymph nodes, reported in five studies,Reference Lee, Lee, Lee, Park, Kim and Son14, Reference Lee, Kwon, Bae and Chung19, Reference Lee, Ryu, Park, Kim, Kang and Jeong38, Reference Lee, Nah, Kim, Ahn, Soh and Chung39, Reference Ryu, Lee, Park, Kang, Jeong and Hong42 was found to be significantly lower in the robotic thyroidectomy group than in the conventional open thyroidectomy group (weighted mean difference = −0.81, 95 per cent CI = −1.32 to −0.29, p = 0.002) (Figure 2b).

Fig. 2 Forest plots displaying (a) operative time and (b) number of retrieved central lymph nodes, comparing robotic thyroidectomy with conventional open thyroidectomy. RT = robotic thyroidectomy; COT = conventional open thyroidectomy; SD = standard deviation; IV = inverse variance; CI = confidence interval

Post-operative outcomes

With respect to complications, eight studies reported transient RLN palsy,Reference Kim, Kang, Kang and Park18Reference Noureldine, Jackson, Tufano and Kandil20, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37Reference Kim, Kim, Hur, Kim, Lee and Choi40 but analysis of the pooled data showed that the two groups (robotic thyroidectomy and conventional open thyroidectomy) did not differ significantly (odds ratio = 1.69, 95 per cent CI = 0.92–3.11, p = 0.09) (Figure 3a). Analysis of the pooled data from the six studies that reported permanent RLN palsyReference Lee, Kwon, Bae and Chung19, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37, Reference Lee, Ryu, Park, Kim, Kang and Jeong38, Reference Kim, Kim, Hur, Kim, Lee and Choi40, Reference Ryu, Lee, Park, Kang, Jeong and Hong42 again revealed no significant difference between the two groups (odds ratio = 9.84, 95 per cent CI = 0.51–191.70, p = 0.13) (Figure 3b). Nine studies reported transient hypocalcaemia,Reference Kim, Kang, Kang and Park18Reference Noureldine, Jackson, Tufano and Kandil20, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37Reference Yi, Yoon, Lee, Sung, Chung and Kim41 which also did not differ significantly between the two groups (odds ratio = 1.08, 95 per cent CI = 0.87–1.34, p = 0.49) (Figure 3c). The pooled data on permanent hypocalcaemia, provided in eight studies,Reference Kim, Kang, Kang and Park18, Reference Lee, Kwon, Bae and Chung19, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37, Reference Lee, Ryu, Park, Kim, Kang and Jeong38, Reference Kim, Kim, Hur, Kim, Lee and Choi40Reference Ryu, Lee, Park, Kang, Jeong and Hong42 also revealed no significant difference between the two groups (odds ratio = 1.00, 95 per cent CI = 0.38–2.65, p = 0.99) (Figure 3d). No significant differences were seen between the two groups regarding chyle leakage (odds ratio = 1.42, 95 per cent CI = 0.57–3.53, p = 0.45) (Figure 3e) or post-operative hospital stay (weighted mean difference = −0.26, 95 per cent CI = −0.61–0.09, p = 0.14) (Figure 3f).

Fig. 3 Forest plots displaying incidences of (a) transient recurrent laryngeal nerve (RLN) palsy, (b) permanent RLN palsy, (c) transient hypocalcaemia, (d) permanent hypocalcaemia and (e) chyle leakage, and (f) duration of post-operative hospital stay, comparing robotic thyroidectomy with conventional open thyroidectomy. RT = robotic thyroidectomy; COT = conventional open thyroidectomy; M-H = Mantel–Haenszel; CI = confidence interval; SD = standard deviation; IV = inverse variance

With regard to oncological outcomes, there was no statistically significant difference in either post-operative suppressed serum thyroglobulin levels (weighted mean difference = 0.07, 95 per cent CI = −0.06–0.20, p = 0.30) (Figure 4a) or in post-operative TSH-stimulated serum thyroglobulin levels (weighted mean difference = 3.05, 95 per cent CI = −3.17–9.27, p = 0.34) (Figure 4b). Three studies reported no tumour recurrences in either the robotic thyroidectomy or conventional open thyroidectomy groups during 12-months' follow up.Reference Lee, Kwon, Bae and Chung19, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37 However, significant heterogeneity among the studies was observed for post-operative hospital stay (I2 = 88 per cent) and post-operative TSH-stimulated serum thyroglobulin levels (I2 = 95 per cent). None of the included studies reported the long-term survival outcome.

Fig. 4 Forest plots displaying (a) post-operative suppressed serum thyroglobulin levels and (b) post-operative thyroid stimulating hormone stimulated serum thyroglobulin levels, comparing robotic thyroidectomy with conventional open thyroidectomy. RT = robotic thyroidectomy; COT = conventional open thyroidectomy; SD = standard deviation; IV = inverse variance; CI = confidence interval

Publication bias

A funnel plot of the studies reporting transient RLN palsy is shown in Figure 5. There was no evidence of publication bias. None of the study findings lay outside the limits of 95 per cent CIs.

Fig. 5 Funnel plot for transient recurrent laryngeal nerve palsy. SE = standard error; OR = odds ratio

Sensitivity and subgroup analysis

Sensitivity analyses were conducted by removing individual studies from the data set. These exclusions did not change the overall results of the analyses. Subgroup analyses were undertaken by including only the higher quality studies. Analysis of the higher quality studies showed results that were similar to those of all studies together, except for the cumulative number of retrieved central lymph nodes. The cumulative numbers of retrieved central lymph nodes were comparable between groups (weighted mean difference = −0.48, 95 per cent CI = −1.23–0.27, p = 0.21). The results of the sensitivity analyses are summarised in Table IV.

Table IV Sensitivity analysis results*

* Only the higher quality studies were analysed. Pts = patients; OR = odds ratio; WMD = weighted mean difference; CI = confidence interval; post-op = post-operative; RLN = recurrent laryngeal nerve

Discussion

Recently, with the improvement of endoscopic apparatus and accumulation of surgical skills, robotic thyroid surgery has gradually been applied to thyroid cancer. However, there seems to be a lack of consensus regarding oncological safety and surgical completeness.Reference Perrier44, Reference Miyano, Lobe and Wright45 To the best of our knowledge, this is the first meta-analysis to compare robotic thyroidectomy with conventional open thyroidectomy for patients with differentiated thyroid cancer.

The results of this meta-analysis showed that operative time was significantly longer in the robotic thyroidectomy group as compared to the conventional open thyroidectomy group, which can be explained by the extra time needed to prepare the working space and robotic docking.Reference Tae, Ji, Jeong, Lee, Jeong and Park7, Reference Lee, Lee, Nah, Soh and Chung46, Reference Kang, Lee, Ryu, Lee, Jeong and Nam47 This result is consistent with previous studies.Reference Lang, Wong, Tsang, Wong and Wan15Reference Sun, Peress and Pynnonen17 We believe that robotic thyroidectomy operative time may decrease with accumulation of the surgeon's experiences and skills.

With regard to lymph node dissection, as one factor of surgical radicalism for malignancy, our results also demonstrated that the robotic thyroidectomy group was associated with significantly fewer retrieved central lymph nodes. This can be attributed to the high degree of patient selection in the robotic thyroidectomy group; in contrast, the conventional open thyroidectomy group comprised more cases of bilateral cancer and multiple central node metastases.Reference Lee, Ryu, Park, Kim, Kang and Jeong38 However, analysis of only the higher quality studies revealed no significant difference in the number of removed central lymph nodes between the two groups. This indicates that the clearance of central lymph nodes achieved by robotic thyroidectomy is similar to that of conventional open thyroidectomy. We attribute this to the magnified, three-dimensional operative views of the robotic system.Reference Lee, Kwon, Bae and Chung19

The major complications of thyroid surgery are RLN palsy and hypocalcaemia. Our results demonstrate no significant differences between the two groups in terms of the incidence rates of transient RLN palsy, permanent RLN palsy, transient hypocalcaemia, permanent hypocalcaemia or chyle leakage. This may largely be a result of the amplified surgical field and excellent apparatus in the robotic system, which enables identification of the RLN, parathyroid gland and thoracic duct.Reference Kim, Kang, Kang and Park18

Oncological outcomes following thyroid cancer, such as completeness of thyroid resection and tumour recurrence, are a concern for surgeons. The findings revealed no significant differences between the two groups in terms of post-operative suppressed serum thyroglobulin levels and TSH-stimulated serum thyroglobulin levels (markers of surgical completeness). This indicates that robotic thyroidectomy can be as complete as conventional open thyroidectomy.Reference Kim, Kim, Hur, Kim, Lee and Choi40 Three studies reported no tumour recurrences during the 12-month follow up.Reference Lee, Kwon, Bae and Chung19, Reference Tae, Song, Ji, Kim, Kim and Choi35, Reference Kang, Lee, Park, Jeong, Park and Lee37 However, none of the studies reported on overall long-term survival. There is still insufficient available data on long-term outcomes to adequately investigate tumour-free survival. Randomised, controlled trials with long-term follow up are needed to more precisely evaluate oncological outcomes following thyroid cancer.

Two of the studies in this analysis reported on cosmetic satisfaction and quality of life,Reference Lee, Nah, Kim, Ahn, Soh and Chung39, Reference Ryu, Lee, Park, Kang, Jeong and Hong42 but the measurements of evaluation were different, making it difficult to pool the results together. Tae et al.Reference Tae, Ji, Cho, Lee, Kim and Kim36 and Lee et al.Reference Lee, Nah, Kim, Ahn, Soh and Chung39 found that cosmetic satisfaction was significantly higher in the robotic thyroidectomy group than in the conventional open thyroidectomy group, because there was no operative scar on the anterior neck and the incision scar in the axilla was almost shaded when the arms were in a natural position.

  • General application of robotic thyroidectomy for malignant thyroid tumours continues to be debated

  • A meta-analysis was conducted to compare short-term outcomes of robotic thyroidectomy and conventional open thyroidectomy for differentiated thyroid cancer

  • The results demonstrated that robotic thyroidectomy is feasible and safe for treating patients with differentiated thyroid cancer

Of course, the meta-analysis has some limitations and hence the results should be interpreted with caution. Firstly, all studies included were non-randomised, observational clinical studies, which might either overestimate or underestimate the measured effect. Secondly, some heterogeneity was observed in certain results between the two groups. This might be explained by differences in patient selection and surgeons' experiences. Thirdly, we were unable to analyse some other important outcomes, such as cosmetic results and quality of life, because of insufficient data. Finally, the follow-up period was short in all studies, and long-term follow-up data are required to properly evaluate the survival of patients with differentiated thyroid carcinoma who undergo robotic thyroidectomy.

In conclusion, the results of this meta-analysis demonstrate that robotic thyroidectomy is feasible and safe for the treatment of patients with differentiated thyroid carcinoma, although robotic thyroidectomy is not superior to conventional techniques with respect to operative time. Further randomised, controlled trials are needed to confirm the effects of robotic thyroidectomy for differentiated thyroid carcinoma patients.

References

1Yang, Y, Gu, X, Wang, X, Xiang, J, Chen, Z. Endoscopic thyroidectomy for differentiated thyroid cancer. Scientific World Journal 2012;2012:456807CrossRefGoogle ScholarPubMed
2Davies, L, Welch, HG. Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA 2006;295:2164–7CrossRefGoogle ScholarPubMed
3Jeryong, K, Jinsun, L, Hyegyong, K, Eilsung, C, Jiyoung, S, Insang, S et al. Total endoscopic thyroidectomy with bilateral breast areola and ipsilateral axillary (BBIA) approach. World J Surg 2008;32:2488–93CrossRefGoogle ScholarPubMed
4Bae, JS, Cho, YU, Sung, GY, Oh, SJ, Jung, EJ, Lee, JB et al. The current status of endoscopic thyroidectomy in Korea. Surg Laparosc Endosc Percutan Tech 2008;18:231–5CrossRefGoogle ScholarPubMed
5Kang, SW, Jeong, JJ, Yun, JS, Sung, TY, Lee, SC, Lee, YS et al. Gasless endoscopic thyroidectomy using trans-axillary approach; surgical outcome of 581 patients. Endocr J 2009;56:361–9CrossRefGoogle ScholarPubMed
6Fan, LJ, Jiang, J. Present and future of robot-assisted endoscopic thyroid surgery. Chin Med J (Engl) 2012;125:926–31Google ScholarPubMed
7Tae, K, Ji, YB, Jeong, JH, Lee, SH, Jeong, MA, Park, CW. Robotic thyroidectomy by a gasless unilateral axillo-breast or axillary approach: our early experiences. Surg Endosc 2011;25:221–8CrossRefGoogle ScholarPubMed
8Ikeda, Y, Takami, H, Sasaki, Y, Takayama, J, Niimi, M, Kan, S. Comparative study of thyroidectomies: endoscopic surgery versus conventional open surgery. Surg Endosc 2002;16:1741–5CrossRefGoogle ScholarPubMed
9Lee, KE, Rao, J, Youn, YK. 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:e715CrossRefGoogle Scholar
10Kandil, EH, Noureldine, SI, Yao, L, Slakey, DP. Robotic transaxillary thyroidectomy: an examination of the first one hundred cases. J Am Coll Surg 2012;214:558–64CrossRefGoogle ScholarPubMed
11Kang, SW, Lee, SC, Lee, SH, Lee, KY, Jeong, JJ, Lee, YS 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;146:1048–55CrossRefGoogle Scholar
12Lee, KE, Kim, E, Koo do, H, Choi, JY, Kim, KH, Youn, YK. Robotic thyroidectomy by bilateral axillo-breast approach: review of 1,026 cases and surgical completeness. Surg Endosc 2013;27:2955–62CrossRefGoogle Scholar
13Kang, SW, Jeong, JJ, Yun, JS, Sung, TY, Lee, SC, Lee, YS et al. Robot-assisted endoscopic surgery for thyroid cancer: experience with the first 100 patients. Surg Endosc 2009;23:2399–406CrossRefGoogle ScholarPubMed
14Lee, S, Lee, CR, Lee, SC, Park, S, Kim, HY, Son, H et al. Surgical completeness of robotic thyroidectomy: a prospective comparison with conventional open thyroidectomy in papillary thyroid carcinoma patients. Surg Endosc 2014;28:1068–75CrossRefGoogle ScholarPubMed
15Lang, BH, Wong, CK, Tsang, JS, Wong, KP, Wan, KY. A systematic review and meta-analysis comparing surgically-related complications between robotic-assisted thyroidectomy and conventional open thyroidectomy. Ann Surg Oncol 2013;21:850–61CrossRefGoogle ScholarPubMed
16Jackson, NR, Yao, L, Tufano, RP, Kandil, EH. Safety of robotic thyroidectomy approaches: meta-analysis and systematic review. Head Neck 2014;36:137–43CrossRefGoogle ScholarPubMed
17Sun, GH, Peress, L, Pynnonen, MA. Systematic review and meta-analysis of robotic vs conventional thyroidectomy approaches for thyroid disease. Otolaryngol Head Neck Surg 2014;150:520–32CrossRefGoogle ScholarPubMed
18Kim, BS, Kang, KH, Kang, H, Park, SJ. Central neck dissection using a bilateral axillo-breast approach for robotic thyroidectomy: comparison with conventional open procedure after propensity score matching. Surg Laparosc Endosc Percutan Tech 2014;24:6772CrossRefGoogle ScholarPubMed
19Lee, J, Kwon, IS, Bae, EH, Chung, WY. Comparative analysis of oncological outcomes and quality of life after robotic versus conventional open thyroidectomy with modified radical neck dissection in patients with papillary thyroid carcinoma and lateral neck node metastases. J Clin Endocrinol Metab 2013;98:2701–8CrossRefGoogle ScholarPubMed
20Noureldine, SI, Jackson, NR, Tufano, RP, Kandil, E. A comparative North American experience of robotic thyroidectomy in a thyroid cancer population. Langenbecks Arch Surg 2013;398:1069–74CrossRefGoogle Scholar
21Stang, A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010;25:603–5CrossRefGoogle ScholarPubMed
22Athanasiou, T, Al-Ruzzeh, S, Kumar, P, Crossman, MC, Amrani, M, Pepper, JR et al. Off-pump myocardial revascularization is associated with less incidence of stroke in elderly patients. Ann Thorac Surg 2004;77:745–53CrossRefGoogle ScholarPubMed
23Higgins, JP, Thompson, SG, Deeks, JJ, Altman, DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–60CrossRefGoogle ScholarPubMed
24Lee, J, Yun, JH, Nam, KH, Choi, UJ, Chung, WY, Soh, EY. Perioperative clinical outcomes after robotic thyroidectomy for thyroid carcinoma: a multicenter study. Surg Endosc 2011;25:906–12CrossRefGoogle ScholarPubMed
25Lee, KE, Koo do, H, Kim, SJ, Lee, J, Park, KS, Oh, SK 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;148:1207–13CrossRefGoogle ScholarPubMed
26Son, H, Park, S, Lee, CR, Lee, S, Kim, JW, Kang, SW et al. Factors contributing to surgical outcomes of transaxillary robotic thyroidectomy for papillary thyroid carcinoma. Surg Endosc 2014;28:3134–42CrossRefGoogle ScholarPubMed
27Kim, JA, Kim, JS, Chang, MS, Yoo, YK, Kim, DK. Influence of carbon dioxide insufflation of the neck on intraocular pressure during robot-assisted endoscopic thyroidectomy: a comparison with open thyroidectomy. Surg Endosc 2013;27:1587–93CrossRefGoogle ScholarPubMed
28Aliyev, S, Taskin, HE, Agcaoglu, O, Aksoy, E, Milas, M, Siperstein, A et al. Robotic transaxillary total thyroidectomy through a single axillary incision. Surgery 2013;153:705–10CrossRefGoogle ScholarPubMed
29Lee, J, Na, KY, Kim, RM, Oh, Y, Lee, JH, Lee, J et al. Postoperative functional voice changes after conventional open or robotic thyroidectomy: a prospective trial. Ann Surg Oncol 2012;19:2963–70CrossRefGoogle ScholarPubMed
30Landry, CS, Grubbs, EG, Warneke, CL, Ormond, M, Chua, C, Lee, JE et al. Robot-assisted transaxillary thyroid surgery in the United States: is it comparable to open thyroid lobectomy? Ann Surg Oncol 2012;19:1269–74CrossRefGoogle ScholarPubMed
31Park, JH, Lee, CR, Park, S, Jeong, JS, Kang, SW, Jeong, JJ et al. Initial experience with robotic gasless transaxillary thyroidectomy for the management of Graves disease: comparison of conventional open versus robotic thyroidectomy. Surg Laparosc Endosc Percutan Tech 2013;23:e173–7CrossRefGoogle ScholarPubMed
32Ji, YB, Song, CM, Bang, HS, Lee, SH, Park, YS, Tae, K. Long-term cosmetic outcomes after robotic/endoscopic thyroidectomy by a gasless unilateral axillo-breast or axillary approach. J Laparoendosc Adv Surg Tech A 2014;24:248–53CrossRefGoogle ScholarPubMed
33Foley, CS, Agcaoglu, O, Siperstein, AE, Berber, E. Robotic transaxillary endocrine surgery: a comparison with conventional open technique. Surg Endosc 2012;26:2259–66CrossRefGoogle ScholarPubMed
34Kim, BS, Kang, KH, Park, SJ. Robotic modified radical neck dissection by bilateral axillary breast approach for papillary thyroid carcinoma with lateral neck metastasis. Head Neck 2015;37:3745Google Scholar
35Tae, K, Song, CM, Ji, YB, Kim, KR, Kim, JY, Choi, YY. Comparison of surgical completeness between robotic total thyroidectomy versus open thyroidectomy. Laryngoscope 2014;124:1042–7CrossRefGoogle ScholarPubMed
36Tae, K, Ji, YB, Cho, SH, Lee, SH, Kim, DS, Kim, TW. 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;34:617–25CrossRefGoogle ScholarPubMed
37Kang, SW, Lee, SH, Park, JH, Jeong, JS, Park, S, Lee, CR et al. A comparative study of the surgical outcomes of robotic and conventional open modified radical neck dissection for papillary thyroid carcinoma with lateral neck node metastasis. Surg Endosc 2012;26:3251–7CrossRefGoogle ScholarPubMed
38Lee, S, Ryu, HR, Park, JH, Kim, KH, Kang, SW, Jeong, JJ et al. Early surgical outcomes comparison between robotic and conventional open thyroid surgery for papillary thyroid microcarcinoma. Surgery 2012;151:724–30CrossRefGoogle ScholarPubMed
39Lee, J, Nah, KY, Kim, RM, Ahn, YH, Soh, EY, Chung, WY. Differences in postoperative outcomes, function, and cosmesis: open versus robotic thyroidectomy. Surg Endosc 2010;24:3186–94CrossRefGoogle ScholarPubMed
40Kim, WW, Kim, JS, Hur, SM, Kim, SH, Lee, SK, Choi, JH et al. Is robotic surgery superior to endoscopic and open surgeries in thyroid cancer? World J Surg 2011;35:779–84CrossRefGoogle ScholarPubMed
41Yi, O, Yoon, JH, Lee, YM, Sung, TY, Chung, KW, Kim, TY et al. Technical and oncologic safety of robotic thyroid surgery. Ann Surg Oncol 2013;20:1927–33CrossRefGoogle ScholarPubMed
42Ryu, HR, Lee, J, Park, JH, Kang, SW, Jeong, JJ, Hong, JY et al. A comparison of postoperative pain after conventional open thyroidectomy and transaxillary single-incision robotic thyroidectomy: a prospective study. Ann Surg Oncol 2013;20:2279–84CrossRefGoogle ScholarPubMed
43Lee, KE, Koo do, H, Im, HJ, Park, SK, Choi, JY, Paeng, JC et al. Surgical completeness of bilateral axillo-breast approach robotic thyroidectomy: comparison with conventional open thyroidectomy after propensity score matching. Surgery 2011;150:1266–74CrossRefGoogle ScholarPubMed
44Perrier, ND. Why I have abandoned robot-assisted transaxillary thyroid surgery. Surgery 2012;152:1025–6CrossRefGoogle ScholarPubMed
45Miyano, G, Lobe, TE, Wright, SK. Bilateral transaxillary endoscopic total thyroidectomy. J Pediatr Surg 2008;43:299303CrossRefGoogle ScholarPubMed
46Lee, J, Lee, JH, Nah, KY, Soh, EY, Chung, WY. Comparison of endoscopic and robotic thyroidectomy. Ann Surg Oncol 2011;18:1439–46CrossRefGoogle ScholarPubMed
47Kang, SW, Lee, SH, Ryu, HR, Lee, KY, Jeong, JJ, Nam, KH et al. Initial experience with robot-assisted modified radical neck dissection for the management of thyroid carcinoma with lateral neck node metastasis. Surgery 2010;148:1214–21CrossRefGoogle ScholarPubMed
Figure 0

Fig. 1 Flow chart showing the process of article identification and selection.

Figure 1

Table I Characteristics of included studies

Figure 2

Table II Quality assessment results*

Figure 3

Table III Meta-analysis results of interest

Figure 4

Fig. 2 Forest plots displaying (a) operative time and (b) number of retrieved central lymph nodes, comparing robotic thyroidectomy with conventional open thyroidectomy. RT = robotic thyroidectomy; COT = conventional open thyroidectomy; SD = standard deviation; IV = inverse variance; CI = confidence interval

Figure 5

Fig. 3 Forest plots displaying incidences of (a) transient recurrent laryngeal nerve (RLN) palsy, (b) permanent RLN palsy, (c) transient hypocalcaemia, (d) permanent hypocalcaemia and (e) chyle leakage, and (f) duration of post-operative hospital stay, comparing robotic thyroidectomy with conventional open thyroidectomy. RT = robotic thyroidectomy; COT = conventional open thyroidectomy; M-H = Mantel–Haenszel; CI = confidence interval; SD = standard deviation; IV = inverse variance

Figure 6

Fig. 4 Forest plots displaying (a) post-operative suppressed serum thyroglobulin levels and (b) post-operative thyroid stimulating hormone stimulated serum thyroglobulin levels, comparing robotic thyroidectomy with conventional open thyroidectomy. RT = robotic thyroidectomy; COT = conventional open thyroidectomy; SD = standard deviation; IV = inverse variance; CI = confidence interval

Figure 7

Fig. 5 Funnel plot for transient recurrent laryngeal nerve palsy. SE = standard error; OR = odds ratio

Figure 8

Table IV Sensitivity analysis results*