A comparative study of the surgical outcomes between video-assisted and open lateral neck dissection for papillary thyroid carcinoma with lateral neck lymph node metastases

    A comparative study of the surgical outcomes between video-assisted and open lateral neck dissection for papillary thyroid carcinoma with lateral neck lymph node metastases Deguang Zhang, Lei Xie, Gaofei He, Liang Fang, Yuwen Miao, Zhezhe Wang, Li Gao PII: DOI: Reference:

S0196-0709(16)30155-7 doi: 10.1016/j.amjoto.2016.07.005 YAJOT 1724

To appear in:

American Journal of Otolaryngology–Head and Neck Medicine and Surgery

Received date:

20 March 2016

Please cite this article as: Zhang Deguang, Xie Lei, He Gaofei, Fang Liang, Miao Yuwen, Wang Zhezhe, Gao Li, A comparative study of the surgical outcomes between videoassisted and open lateral neck dissection for papillary thyroid carcinoma with lateral neck lymph node metastases, American Journal of Otolaryngology–Head and Neck Medicine and Surgery (2016), doi: 10.1016/j.amjoto.2016.07.005

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ACCEPTED MANUSCRIPT A comparative study of the surgical outcomes between video-assisted and open lateral neck dissection for papillary thyroid carcinoma with lateral neck lymph

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node metastases

Deguang Zhanga, Lei Xiea, Gaofei Hea, Liang Fanga, Yuwen Miaoa, Zhezhe Wanga,

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Li Gaoa

Head and Neck Surgery Department of SIR RUN RUN SHAW Hospital, Institute of

Corresponding author: Li Gao E-mail: [email protected]

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Micro-Invasive Surgery of Zhejiang University, Hangzhou, P.R. China, 310016.

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Disclosure: None of the authors have any potential conflicts of interest associated

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with this research.

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ACCEPTED MANUSCRIPT Abstract PURPOSE: Video-assisted lateral neck dissection (VALND) for papillary thyroid

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carcinoma (PTC) with lateral neck lymph node metastases (LNM) has been described previously, however, the advantages and drawbacks of VALND have not been

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demonstrated in previous studies. The aim of this study was to compare the surgical outcomes of video-assisted and open lateral neck dissection for PTC with lateral neck

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LNM.

MATERIALS AND METHODS: Between May 2013 and November 2014, 92 consecutive patients with PTC and lateral neck lymph node metastases underwent

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total thyroidectomy with central compartment neck dissection and unilateral lateral

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neck dissection. These included 54 individuals who underwent video-assisted surgery, and 38 in whom an open approach was used. The two groups were retrospectively

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compared with respect to their clinicopathological characteristics, surgical outcomes

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and oncological completeness. RESULTS: The mean follow-up period was 18.6 months. The mean tumor size, tumor stage, mean numbers of retrieved lymph nodes, mean postoperative serum thyroglobulin levels, complication rates, and mean postoperative hospital stay were similar between the two groups. The mean operation time was longer (p=0.0001) and mean age was lower (p=0.0354) in the video-assisted group. The cosmetic results, evaluated by numerical scale and verbal response scale, was in favor of the video-assisted group (p = 0.0003 and p < 0.0001, respectively). CONCLUSIONS: The safety and oncological completeness of VALND was similar 2

ACCEPTED MANUSCRIPT to that of open procedures, but the VALND resulted in improved cosmetic results. VALND is an effective treatment for the selected cases of PTC with lateral neck

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LNM.

Key words Cosmetic results; Lateral neck dissection; Papillary thyroid carcinoma;

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Video-assisted

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ACCEPTED MANUSCRIPT 1. Introduction Papillary thyroid carcinoma (PTC) is the most common type of thyroid malignancy

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and is the most likely to metastasize to the regional lymph nodes [1]. Therapeutic lateral neck dissection (LND) is recommended in patients with clinical evidence of

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lymph node involvement of the lateral neck compartment [2]. Although open LND is the standard approach, it inevitably yields poor cosmetic results, due to a long scar on

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the neck. To avoid producing a long anterior neck scar in PTC patients, several studies have used video-assisted LND (VALND), and the feasibility of VALND has been confirmed [3-6], but the advantages and drawbacks of VALND have not been

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demonstrated in previous studies. In this study, we compared the surgical outcomes

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between VALND and open LND for PTC with lateral neck lymph node metastases

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(LNM).

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2. Materials and methods 2.1 Patients

We retrospectively assessed a cohort of consecutive patients with PTC and lateral neck LNM who underwent total thyroidectomy with central compartment neck dissection (CCND) and unilateral LND at the Head and Neck Surgery Department of SIR RUN RUN SHAW Hospital, Institute of Micro-Invasive Surgery of Zhejiang University from May 2013 to November 2014. Of those patients, 54 underwent a video-assisted (VA) approach and 38 underwent an open approach. Preoperative diagnoses and staging were revealed by ultrasonography (US), computed tomography 4

ACCEPTED MANUSCRIPT (CT), and ultrasound-guided fine needle aspiration biopsy (FNAB) examination. The presence of lateral neck LNM was determined by ultrasound-guided FNAB and

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histology examinations preoperatively. Levels II, III, IV and Vb dissection were performed routinely in all cases. Before inclusion into the study, patients had to meet

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certain inclusion and exclusion criteria. The inclusion criteria were: (1) primary tumor size ≤ 4.0 cm, (2) largest diameter of the metastatic lymph node ≤ 2.5 cm, and (3) ≤ 2

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levels LNM in the lateral neck compartment by US and CT examinations preoperatively. The exclusion criteria were: (1) a history of previous neck surgery; (2) metastatic lymph nodes at level I or Va; (3) ≥ 3 levels of LNM in the lateral neck

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compartment by US and CT examinations preoperatively; (4) primary tumor or

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metastatic lymph node invasion into major vascular structures, the trachea, or the esophagus. The choice of VA or open approach was made on patients’ cosmetic

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demands and economic status. All patients signed a written informed consent form,

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and our institutional review board approved this study.

2.2 Surgical procedures Under general endotracheal anesthesia, patients were placed in a supine position with the neck slightly extended by a roll placed beneath the shoulders and a small donut placed under the occiput to stabilize and support the head. 2.2.1 VALND procedure A single 4-cm to 5-cm transverse incision was made in the central region of the neck about 1-finger breadth above the sternal notch, in the natural skin folds. After a total thyroidectomy and CCND were performed under a direct visual field approach, 5

ACCEPTED MANUSCRIPT the patient’s head was turned to the opposite side from the lesion to expose the lateral neck compartment area, and LND was performed via the VA approach. The

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procedures used for VALND were similar to those reported by Lombardi et al. [3] and Miccoli et al. [4], but with some modifications. The first is the working space creation

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technique. In China, a self-developed working space creator (Hangzhou Good Grams Photoelectric Instrument Co. Ltd., Hangzhou, China) has been invented and widely

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used for minimally invasive VA thyroidectomy (MIVAT) [7]. Based on our experience with MIVAT, we have used this working space creator in the VALND procedure. Instead of having an assistant using manual retraction to create space, the working

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space creator can mechanically elevate the upper skin flap and keep the working

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space stable for a long time. The second technique used is a negative-pressure suction device that is attached to the long retractor (Hangzhou Good Grams Photoelectric

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Instrument Co. Ltd., Hangzhou, China), supplying continuous suction to remove the

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steam that was generated by the Harmonic scalpel (Ethicon Endo-Surgery, Cincinnati, OH, USA), to ensure clear visibility during surgery (Fig. 1A, B). An upper flap was created and lifted using the self-developed working space creator consisting of a long retractor fitted with a suction apparatus. The tent-like working space created in this way provided a large, stable area for simultaneous insertion of a 10-mm, 30-degree endoscope and surgical instruments through the same skin incision. The steam generated by the Harmonic scalpel was cleared immediately using the continuous negative-pressure suction apparatus connected to the long retractor. Then, the medial border of the SCM, with fascia, was dissected and retracted by one long retractor. 6

ACCEPTED MANUSCRIPT Another long retractor could be repositioned as needed, depending on the dissection location (Fig. 2). The carotid sheath was opened, and the internal jugular vein (IJV)

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and carotid artery were exposed between the carotid bifurcation (cranially) and the subclavian vessels (caudally). The IJV was retracted medially with a long retractor,

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the vagus nerve was exposed, and the lymph nodes and surrounding fibroadipose tissue were retracted and dissected downward. The spinal accessory nerve (SAN),

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cervical plexus, phrenic nerve, and brachial plexus were exposed and preserved, as was the transverse cervical artery. The thoracic duct on the left side or the right lymphatic duct could be identified and preserved in some cases due to the

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magnification provided by the endoscope; they were ligated safely when necessary.

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The lateral neck lymph nodes were resected en bloc (Fig. 3).

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2.2.2 Open LND procedure

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A 9-cm to 12-cm extended collar incision was made along the natural skin fold about one finger breadth above the sternal notch. The skin flap was made to the hyoid bone superiorly, the superior edge of the clavicle inferiorly, and the anterior edge of the trapezius posteriorly. After a total thyroidectomy and CCND, the patient’s head was turned to the opposite side of the lesion to improve the exposure of the lateral neck compartment area. Then, the medial border of the SCM with fascia was dissected and retracted laterally. The carotid sheath was opened, and the IJV and carotid artery were exposed between the carotid bifurcation (cranially) and subclavian vessels (caudally). The SAN, cervical plexus, phrenic nerve, and brachial plexus were exposed and 7

ACCEPTED MANUSCRIPT preserved, along with the transverse cervical artery. The lateral neck lymph nodes were resected en bloc.

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2.3 Postoperative follow-up

All patients were treated with 100 mCi radioactive iodine (RAI) from 2 to 4 months

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postoperatively. All patients also received suppressive levothyroxine therapy. Direct or indirect laryngoscopy was performed pre- and postoperatively to assess vocal cord

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function. Serum thyroglobulin (sTg) and thyroglobulin antibody levels were measured every 6 months after surgery. Ulrasonography was performed to assess the thyroid bed and lateral neck compartment every 6 months after surgery. Cosmetic results were

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evaluated on a numerical scale and a verbal response scale [8]. The numerical scale

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ranged from 0 to 10, with a higher score indicating a better cosmetic result. The verbal response scale included four options: 1 = poor; 2 = acceptable; 3 = good; and 4

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= excellent. All patients were asked to grade the cosmetic appearance of their skin

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incision at 1 year after surgery.

2.4 Statistical analysis Statistical analysis was conducted using Statistical Analysis System, version 9.0 (SAS Inc., Cary, NC, USA). The results were expressed as mean ± standard deviation (SD). Statistical significance was defined as p < 0.05.

3. Results The clinicopathological characteristics of the two groups are summarized in Table 1. 8

ACCEPTED MANUSCRIPT The VA group included 54 patients (15 men and 39 women) with a mean age of 39.1 ± 10.0 years (range: 19–56 years). The open approach group included 38 patients (14

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men and 24 women) with a mean age of 44.1 ± 10.9 years (range: 23–64 years). The mean age was lower in the VA group than in the open group (p = 0.0354). The two

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groups were similar in terms of gender ratio, mean tumor size, tumor multiplicity and tumor bilaterality. Although the duration of surgery was 198.8 ± 19.6 min for the VA

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group and 172.3 ± 28.0 min for the open group (p = 0.0001), there was no significant difference between the two groups in terms of the duration of postoperative hospital stay. The mean retrieved numbers of central and lateral lymph nodes were similar

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between the two groups. Cosmetic results were significantly better in the VA group

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than in the open group as assessed both on the numerical scale (p = 0.0003) and the verbal response scale (p < 0.0001) (Table 1).

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The complication rates were similar between the two groups (Table 2). No cases

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of permanent hypocalcemia, recurrent laryngeal nerve (RLN) injury (except the cases where the RLN was sacrificed due to cancer invasion), or Horner’s syndrome were observed in either group. Two cases of minor chyle leakage (one in the VA group and one in the open group) were observed, and these successfully responded to conservative management. One case of major chyle leakage was observed in the open group, and reoperation was performed to ligate the left lymphatic ducts. One case of postoperative hematoma formation was observed in each group. Postoperative sTg levels (TSH suppressed) remained <1 ng/mL in all patients at 1 year postoperatively. The mean sTg level on LT4 was 0.06 ± 0.10 ng/mL (range: 0– 9

ACCEPTED MANUSCRIPT 0.52 ng/mL) in the VA group and 0.06 ± 0.09 ng/mL (range: 0–0.34 ng/mL) in the open group; there was no significant difference between the two groups (Table 3). The

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mean follow-up period was 18.6 months (range: 12–30 months) and neck ultrasonography showed no evidence of residual tumor or recurrence in any of these

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patients.

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4. Discussion

Traditional neck dissection for PTC with lateral neck LNM requires a long cervical incision, such as an L-shaped, U-shaped, or extended collar incision, which leaves a

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long scar on the neck. Because most PTC patients are young or middle-aged women,

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it is challenging for thyroid surgeons to shorten or eliminate the anterior neck scar in order to meet the patients’ cosmetic demands. A scarless-neck approach, via the breast

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and anterior chest, has been reported for PTC with ipsilateral LND [9]. However, the

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application of this approach for thyroid carcinoma may result in tumor seeding or local recurrence around the operative bed, due to poor technique, such as excessive manipulation, carbon dioxide insufflation-related spillage, or the “chimney effect” [10,11]. Moreover, given the connection between the manubrium of the sternum and the clavicle, it should be questioned whether lymph node dissection is complete when metastatic lymph nodes are located in the anterosuperior mediastinum (level VII) or corner region (level IV, where the IJV joins the subclavian vein). Kang et al. [12] and Lee et al. [13] described a robotic transaxillary approach for performing a modified radical neck dissection for PTC, with which they achieved a similar early surgical 10

ACCEPTED MANUSCRIPT outcome and oncological completeness as with the conventional open modified radical neck dissection. The use of articulated instruments in the robotic approach

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may allow level VII and corner area dissection, but the cost of the robotic system limits the application of this procedure to few specialized centers.

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Several VALND approaches have been described previously [4-6, 14], and it seems to be more suitable for thyroid malignancies with lateral neck LNM than for

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other endoscopic techniques. The VA procedure is similar to the open procedure, which makes it less technically demanding and time-consuming. However, in previous reports, the working space for the VA approach was maintained by two

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manual retractors managed by an assistant; in our experience, that space is small and

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unstable. During complex and difficult procedures, such as LND, particularly level II dissection, it is difficult to perform endoscopic surgery according to the principles of

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oncologic safety, and thus operative maneuvers may be limited. Therefore, we

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modified the working space creation procedure of the VALND. Instead of having an assistant using manual retraction to create space, the working space creator can mechanically elevate the upper skin flap and keep the working space stable for a long time, which can assist the surgeon to continue with the procedure and thereby guarantee the safety of the surgical procedure. Moreover, a wider working space was gained by our approach, as three retractors were used to maintain the working space. Therefore, the lateral neck lymph nodes could be dissected easily in a relatively large and stable surgical working space. The level II dissection (especially level IIb dissection) is very difficult when the patients’ neck is long and/or wide through the 11

ACCEPTED MANUSCRIPT inferior neck extended collar incision. However, the widely endoscopic exposure of the neck structures can makes the level II dissection safer and easier.

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The limitations of the minimally invasive approach for thyroid surgery are the longer duration of surgery and higher overall costs. In terms of the learning curve of

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VALND, 20 patients represented the early stage of the learning curve, and 40 patients represented the number of procedures required to reach an advanced level of skill.

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The operation time will be significantly longer than the conventional open approach at the beginning of the surgeon’s experience. This could probably mean higher cost in terms of operating room usage in the VA approach. In this study, the time for surgery

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by VALND was longer （ about 26 minutes ） than for the open approach,

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improvement in surgical proficiency can lead to a decreased operation time by VALND, and now the operation time is comparable to the open approach and the

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overall cost does not increase dramatically.

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Some surgeons are still skeptical about the oncological completeness of the endoscopic approach because PTC with LNM is a locally advanced disease. It is difficult to perform endoscopic surgery according to the principles of oncologic completeness when a complex and difficult procedure like LND is performed. However, with the improvement of surgical instruments by means of endoscope magnification, a compartment-oriented anatomical dissection could be performed and LND with oncologic principles is possible. Similarly, the results of this study show that there was no significant difference in the numbers of central and lateral compartment lymph nodes retrieved or the postoperative sTg level. Furthermore, 12

ACCEPTED MANUSCRIPT although the follow-up period was short, no local recurrence or residual was detected by high-resolution US in all patients.

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In terms of cosmetic result, it seems reasonable that a 4-cm to 5-cm anterior neck scar is superior to a 9-cm to 12-cm incision scar. Moreover, a symmetrical neck

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incision meets esthetic demands. In this study, the cosmetic result was evaluated on a numerical scale and a verbal response scale, and both favored the VA approach.

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The major limitation of this study is that it was not a case-matched study and the age was not matched between the two groups. In this study, the mean age was lower in the VA group, but the T, N, M classifications and tumor stage was similar between

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the two groups. So, this comparative study of the oncological completeness between

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5. Conclusions

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the two groups is acceptable.

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In summary, we found that VALND yielded safety and oncological completeness similar to that of open procedures, however, VALND resulted in better cosmetic results. Accordingly, we suggest that a retrospective case-matched study or prospective randomized controlled study should be conducted to confirm our findings.

6. Acknowledgement No

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ACCEPTED MANUSCRIPT References [1] Bhattacharyya N. Surgical treatment of cervical nodal metastases in patients with

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papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg 2003; 129: 1101–4. [2] Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, et al.

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American Thyroid Association Guidelines Taskforce. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2006; 16:

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109–42.

[3] Lombardi CP, Raffaelli M, Princi P, De Crea C, Bellantone R. Minimally invasive video-assisted functional lateral neck dissection for metastatic papillary thyroid

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carcinoma. Am J Surg 2007; 193: 114–8.

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[4] Miccoli P, Materazzi G, Berti P. Minimally invasive videoassisted lateral lymphadenectomy: a proposal. Surg Endosc 2008); 22: 1131–4.

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[5] Wu B, Ding Z, Fan Y, Deng X, Guo B, Kang J, et al. Video-assisted selective

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lateral neck dissection for papillary thyroid carcinoma. Langenbecks Arch Surg 2013; 398: 395–401.

[6] Zhang Z, Xu Z, Li Z, An C, Liu J, Zhu Y, et al. Minimally-invasive endoscopically-assisted neck dissection for lateral cervical metastases of thyroid papillary carcinoma. Br J Oral Maxillofac Surg 2014; 52: 793–7. [7] Li G, Ying H, Yan S, Song CY, Xiao GZ, Li H, et al. Application of Miccoli’s endoscopic thyroidectomy with technical modifications--a report of 530 cases. J Surg Concepts Pract 2004; 9: 4705 (in Chinese). [8] Miccoli P, Berti P, Raffaelli M, Materazzi G, Baldacci S, Rossi G. Comparison 14

ACCEPTED MANUSCRIPT between minimally invasive video-assisted thyroidectomy and conventional thyroidectomy: A prospective randomized study. Surgery 2001; 130: 103943.

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[9] Li Z, Wang P, Wang Y, Xu S, Cao L, Que R, et al. Endoscopic lateral neck dissection via breast approach for papillary thyroid carcinoma: a preliminary report.

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Surg Endosc 2011; 25: 890–6.

[10] Huang CP, Ji QH, Li RS, Zhu YX. Analysis of four cases of inappropriate

2008; 46: 416–7 (in Chinese).

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application of endoscopic thyroidectomy to thyroid cancer. Zhonghua Wai Ke Za Zhi

[11] Kim JH, Choi YJ, Kim JA, Gil WH, Nam SJ, Oh YL, et al. Thyroid cancer that

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developed around the operative bed and subcutaneous tunnel after endoscopic

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thyroidectomy via a breast approach. Surg Laparosc Endosc Percutan Tech 2008; 18: 197–201.

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[12] Kang SW, Lee SH, Park JH, Jeong JS, Park S, Lee CR, et al. A comparative

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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: 3251–7. [13] Lee 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: 2701–8. [14] Ikeda Y, Takami H, Sasaki Y, Takayama J, Kan S, Niimi M. Minimally invasive video-assisted thyroidectomy and lymphadenectomy for micropapillary carcinoma of 15

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the thyroid. J Surg Oncol 2002; 80: 218–21.

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Figure Legends

Fig. 1 A. The system used for creating working space included a self-developed

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working space creator (W) and three long retractors (R). B. The self-developed space creating system in practical use. S, suction apparatus. Fig. 2 The surgical field after lateral neck dissection and the working space was

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maintained by the self-developed working space creator and three long retractors. CB,

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carotid bifurcation; IJV, internal jugular vein; M, muscle; N, nerve; SAN, spinal accessory nerve; SCM, sternocleidomastoid muscle.

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Fig. 3 The operative incision (5.0cm length) after VALND and the lymph nodes

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were resected en bloc.

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Open group

(N = 54)

(N = 38)

39.1 ± 10.0

44.1 ± 10.9

Age range (years)

1956

2364

Male:female

15:39

LND side (left: right)

P value

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0.0354

0.3568

27:27

21:17

0.6188

Operation time (min)

198.8 ± 19.6

172.3 ± 28.0

0.0001

Postoperative hospital

5.2 ± 2.3

0.3834

1.31 ± 0.81

1.64 ± 1.10

0.2591

multiplicity

27:27

23:15

0.3183

bilaterality

21:33

14:24

0.8422

13.3 ± 7.1

12.1 ± 7.4

0.2286

4.8 ± 1.6

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stay (days)

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Tumor size (cm)

Tumor

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14:24

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Age (years)

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VA group

(yes/no)

Tumor (yes/no)

Number of retrieved LN

Central

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Lateral

43.8 ± 13.1

T1/T2/T3/T4a

34/3/15/2

N0/N1a/N1b

0/0/54

0/0/38

54/0

38/0

37/17

19/19

0.0731

6.1 ± 1.3

0.0003

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compartment

TNM classifications

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Tumor stage I/IV

Numeric scale

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Verbal response scale

18/2/14/4

0.3666

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M0/M1

Cosmetic result

0.3194

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41.1 ± 12.9

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compartment

7.0 ± 1.2

2.7 ± 0.6

2.0 ± 0.7

< 0.0001

Table 1 Clinicopathological characteristics and cosmetic results of the patients in the two study groups LND: Lateral neck dissection; LN: Lymph node; VA: Video-assisted

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Open group

(N = 54)

(N = 38)

Transient hypocalcemia

9

5

Permanent hypocalcemia

0

Transient hoarseness

4

Permanent hoarseness

0

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0

1

0.4130

1

1

1.0000

1

2

0.5670

1

1

1.0000

0

1

0.4130

1

0

1.0000

1

0

1.0000

1

1

1.0000

Hematoma formation Chyle leak

Major

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Wound infection

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Minor

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Horner’s syndrome

RLN sacrifice due to

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P value

0.7720

0 3

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Seroma formation

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VA group

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0

cancer invasion

Table 2 Comparison of complications in the two study groups RLN: Recurrent laryngeal nerve; VA: Video-assisted

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1.0000

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Open group

(N = 54)

(N = 38)

P value

Postoperative sTg level

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VA group

0.06 ± 0.10

0.06 ± 0.09

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at 1 year (ng/mL, TSH

0.8704

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suppressed)

Postoperative sTg

0/54

level > 1ng/ml at 1 year

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(TSH suppressed)

0/38

0/54

0/38

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Local recurrence or

US

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residual at follow-up

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Table 3 Comparison of oncological completeness in the two study groups sTg: Serum thyroglobulin; VA: Video-assisted

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Fig. 1

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Fig. 2

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Fig. 3

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