Introduction

The quality of life (QOL) has recently become one of the most important issues for many people. In relation to medical treatment, especially surgical procedures, the severity of pain, the cosmetic outcome, and the loss of activity after surgery are important. Compared with males, thyroid disease is much more common among females, especially young women; thus, a good cosmetic outcome after thyroid surgery tends to be desirable. However, conventional open thyroidectomy creates a long scar and may lead to keloid formation in the midline of the neck with an impairment of the QOL. Operations performed via a small incision, including endoscopic surgery, were subsequently developed as a means of overcoming these problems.

Endoscopic thyroid surgery was first reported by Gagner et al. in 1996 [1], and video-assisted thyroid resection was reported by Hüscher et al. in 1997 [2]. Over time, various techniques and devices for endoscopic thyroidectomy have been reported with good results. Recently, endoscopic thyroidectomy with robotic surgery (da Vinci; Intuitive Surgical, Sunnyvale, CA, USA) has also been performed in some institutions [3–5]. Our institute has started performing a simple and safe method of endoscopic thyroidectomy using the Lap-protector and E·Z-access, referred to as E·Z-access using video-assisted neck surgery (EZ-VANS). We herein report the safety and efficacy of this method for thyroid tumors, including early-stage thyroid cancer.

Methods

Patients and surgeons

A total of 140 thyroid operations were performed from January 2007 to September 2014 in our hospital. The operation was performed with a cervical collar incision (open surgery) in 73 cases, while endoscopic thyroidectomy procedures were used in 67 patients. Operations based on the VANS method reported by Shimizu et al. [6, 7] were carried out in 30 patients from January 2007 to January 2010. We developed endoscopic thyroidectomy using the EZ-VANS system and performed 37 procedures from February 2010 to September 2014. The study protocol was approved by the Ethics Committee at the University of Toyama, and all patients provided their informed consent prior to undergoing thyroid operation. In this facility, thyroid operations with open surgery were performed by a total of 3 senior resident surgeons, and all the VANS and EZ-VANS operations were performed by one surgeon.

Diagnosis of thyroid tumor

The thyroid tumors were diagnosed before operation by an aspiration needle biopsy under ultrasound guidance. If the pathological diagnosis was class III/IV, then the tumor size, number of nodules, invasion of the capsule, spread to the opposite lobe, and lymph node metastasis were investigated.

Indication of endoscopic thyroidectomy

The indications for endoscopic thyroidectomy were as follows: (1) the thyroid lesion was diagnosed as a follicular tumor of Class III or more by a biopsy, (2) the diagnosis was papillary carcinoma with a low risk, or (3) the patient preferred an endoscopic operation due to the cosmetic outcome or an effect on the symptoms. Patients with extensive cancer invasion into the muscles or trachea beyond the thyroid capsule, with multiple lymph node metastases outside the cervical region (Nos. V, VI, or VII), and with distant metastasis detected by US, CT, thyroid scintigraphy, and/or FDG-PET were excluded. Patients who had multiple cervical lymph node metastases with invasion of the recurrent laryngeal nerve were also excluded. Ipsilateral cervical lymph node dissection for the prevention of recurrence was performed in all patients with malignant tumors. These procedures were based on the 1st edition of the treatment guideline developed at a Japanese thyroid surgery meeting [6]. We investigated the operating time in each case, amount of bleeding, duration of hospitalization after surgery, frequency of complications, diameter of the tumor, and pathological diagnosis. We also investigated the TNM classification according to the American Cancer Society and International Union Against Cancer (AJCC/UICC) criteria, as well as the 15th edition of the thyroid cancer handling rules. All of the patients with thyroid cancer took Tyradin/levothyroxine (TSH antagonist) after surgery and underwent follow-up examinations every 3–6 months. The average observation period was 22.5 months (5–63 months).

Operative method of EZ-VANS

The patient was placed in the face-up position under general anesthesia. The neck was not extended and a low pillow was put under the head. The arm on the involved side was lifted up to expose the axillary region. Then, a skin incision of 4 cm was made in the axillary region to insert the Lap-protector mini (LP: Hakkou Shoji, Japan). From the axillary incision, the pectoralis major was dissected using an electric knife. The sternocleidomastoid (SCM) muscle was detached between the head of the clavicle and the sternum to expose the sternohyoid (SH) muscle. The SH and sternothyroid (ST) muscles were partially dissected to expose the thyroid gland. Two Kirschner wires were inserted in parallel under the neck skin between the upper and lower poles of the thyroid, and the skin flap was hung up to create a working space. Because the SCM attached to the skin was also hung up with the skin flap, it made it easy to view the thyroid tumor in the back of the SCM. The LP was inserted through the axillar incision, and it was covered with an E·Z-access (Hakkou Shoji, Japan). Then, 3 ports of 5 mm in diameter (E·Z-ports; 2 ports of 9 cm in length and 1 port of 5 cm in length) were placed for the forceps, Harmonic scalpel, and 5 mm flexible endoscope (Fig. 1a, b). When necessary, a small incision was made and another 5 mm port was placed at the edge of the neck to observe the upper pole of the thyroid gland endoscopically. This wound creates a small scar that is inconspicuous. Surgery was performed using the typical thyroid resection procedure. The coagulation incision of the suprathyroid artery and vein was performed using the Harmonic scalpel and the upper pole of the thyroid gland was elevated to avoid damage to the outer branch of the supralaryngeal nerve. The parathyroid gland in the upper pole was identified and retained after thyroid resection. The middle and lower thyroid vessels were transected in turn, and the thyroid gland was rolled up (Fig. 1c). Then, the thyroid was pulled in the proximal direction and the ligament of Berry was peeled off. The thyroid was transected at the isthmus. Careful resection was performed to protect the recurrent laryngeal nerve. The recurrent laryngeal nerve was checked with the NIM monitor along its full length. The dissected specimen was extracted through the axillary incision. A closed-type drain of 3 mm diameter was placed at the site of resection and the skin was carefully closed with subcutaneous sutures using 4-0 PDS-II.

Fig. 1
figure 1

Devices and methods using in the EZ-VANS operation. a A Lap-protector was covered with an EZ-Access. Three EZ-ports (2 ports of 9 cm length and 1 port of 5 cm length) were placed through the EZ-Access. b The Lap-protector, EZ-access and EZ-ports were inserted from the small axillar incision and set as shown. The neck skin flap was raised up to create a working space. c An illustration of endoscopic thyroidectomy. The lower thyroid vessels were transected and the thyroid gland was rolled up. d The wound after EZ-VANS operation. A small wound is shown in the right axillar of a patient. No other wounds were visible. LP Lap-protector, EA EZ-Access, EP EZ-port, SCM sternocleidomastoid muscle, SH sternohyoid muscle

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Statistical analysis

Matching and statistical analyses were performed using the JMP11.0 software program. Continuous variables were compared using the Mann–Whitney U test. Fisher’s exact test was used for the comparison of categorical variables. Values of p < 0.05 were considered to be statistically significant.

Results

There were 110 cases of open and EZ-VANS thyroidectomy, including 40 patients with benign thyroid tumors (20 had open surgery and 20 had EZ-VANS) and 70 patients with malignant tumors (53 had open surgery and 17 had EZ-VANS; p < 0.001). The benign:malignant ratio was 1:1.75 (Table 1). The average age of the Open and EZ-VANS groups was 58.5 and 51.3 years, respectively, and the EZ-VANS group was younger than the Open group (p = 0.016). The Open group included 21 (28.8 %) males and 52 (71.2 %) females, while the EZ-VANS group had 5 (13.5 %) males and 32 (86.5 %) females (p = 0.097). Symptoms were noted before the operation in 28 patients (38.4 %) from the Open group and 13 patients (35.1 %) from the EZ-VANS group. In the benign, Open group, nine cases complained of thyroid tumor, and one case complained of neck discomfort. In the malignant, Open group, eight cases complained of thyroid tumor, six of neck discomfort, three of neck pain and one patient went to the hospital for a checkup of hives. In the benign, EZ-VANS group, four cases complained of thyroid tumor, two of general fatigue, and one of mouth dryness. In the malignant, EZ-VANS group, two cases complained of thyroid tumor, two of general fatigue, and two of neck discomfort and an edema of the legs. More patients with symptoms of thyroid tumor were observed in the benign group compared with the malignant group; however, there was no significant difference between the two groups. The average number of nodules was 1.31 in the Open group and 1.05 in the EZ-VANS group. Thus, the number of nodules was increased in the Open group overall (p = 0.015), however, there was no significant difference between each benign and malignant group (p = 0.076 and 0.106; Table 1). Among the 110 patients, 75 thyroid tumors were excised with the removal of one lobe, including 50 tumors (75.3 %) in the Open group and 37 tumors (100 %) in the EZ-VANS group. The tumor involved both lobes in 18 (24.7 %) patients, all of whom were in the Open group (Table 2). Partial thyroidectomy was performed in 28 benign tumor patients, including 10 from the Open group (13.7 %) and 18 from the EZ-VANS group (48.6 %), and the partial resection rate of the EZ-VANS group was higher than that of the Open group (p = 0.014). In the operations for malignant tumor, the partial resection rate was similar between the Open and EZ-VANS groups (p = 0.149). Thyroid lobectomy and total thyroidectomy were performed in 42 and 18 patients from the Open group (57.5 and 24.7 %), respectively. Sixteen patients in the EZ-VANS group (43.2 %) underwent thyroid lobectomy, and none of them underwent total thyroidectomy (Table 2).

Table 1 Demographics and extent of surgery in patients with thyroid tumors treated by Open and EZ-VANS operations (n = 110)
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Table 2 Comparison between the operations and the perioperative outcomes between patients with benign or malignant thyroid tumors treated using Open or EZ-VANS operations (n = 110)
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The average diameter of the resected benign tumor was nearly significantly different between the Open group (43.1 mm; area 8–150 mm) and the EZ-VANS group (26.6 mm; area 10–50 mm) (p = 0.058). In patients with malignant tumors, the diameter of the resected tumor showed no difference between the Open and EZ-VANS groups (p = 0.268; Table 2). The median operating time of the Open group was 159 ± 74 min, while it was 172 ± 79 min in the EZ-VANS group, and there was no significant difference in the operating time between the two groups (p = 0.102). In both the benign and malignant thyroid tumor operations, the operating time of the Open group (133 ± 65 min and 147 ± 47 min, respectively) and EZ-VANS group (154 ± 60 min and 182 ± 45 min, respectively), also showed no differences (p = 0.067 and p = 0.13, respectively; Table 2). The average amount of bleeding was 56.5 ml in the Open group and 54.7 ml in the EZ-VANS group, and there was no apparent difference (p = 0.82). In both the benign and malignant thyroid tumor operations, the amount of bleeding in the Open group (46.5 and 59.4 ml, respectively), and EZ-VANS group (54.7 and 48.5 ml, respectively), also showed no difference (p = 0.67 and p = 0.59, respectively). The duration of hospital stay after surgery was 6.7 ± 1.7 days (range 3–30 days) in the Open group and 5.6 ± 0.9 days (range 3–7 days) in the EZ-VANS group (p = 0.28). Additionally, no difference was observed in the hospital stay between the benign and malignant tumor operation cases (p = 0.096 and p = 0.26, respectively). Six side effects occurred after thyroidectomy in the Open group and one occurred in the EZ-VANS group (p = 0.35). In the Open group, postoperative bleeding was detected in one patient with a benign tumor (1.6 %), and the other five complications were detected in the malignant tumor group (8.1 %). Bronchial edema was observed in two cases (one each in the Open and EZ-VANS groups).

The correlation between surgical experience and the operating time was examined in the EZ-VANS and Open groups, and the learning curve for the acquisition of the EZ-VANS method was compared with that of open surgery. The correlation coefficient of all cases was K = −0.98 and K = −0.38 in the EZ-VANS and Open groups, respectively. In benign tumor cases, the correlation coefficient was K = −1.2 and K = −0.3 in the EZ-VANS and Open groups, respectively. In malignant tumor cases, it was K = −0.53 and K = −0.4, respectively. These findings suggest that the time required for the acquisition of the EZ-VANS method was shorter than that for the open method, and it was more obvious in the benign tumor group compared with the malignant group (Fig. 2).

Fig. 2
figure 2

The learning curve for acquisition of the EZ-VANS and open surgery methods. The time periods (minutes) of total tumor (n = 110), benign tumor (n = 43) and malignant tumor (n = 67) were examined and the correlation coefficient of EZ-VANS and Open were compared

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Discussion

The operation of thyroid and parathyroid glands is important for controlling various thyroidal or parathyroid diseases [7, 8]. With the development of laparoscopic surgical techniques and instruments, various procedures for endoscopic thyroidectomy have been reported. Shimizu et al. [9, 10] reported a procedure for gasless video-assisted neck surgery (VANS). Bellantone et al. [11] reported the use of video-assisted thyroid lobectomy with a minimal neck incision. In addition, Ikeda et al. reported endoscopic thyroidectomy via the axillary approach [12–15]. Furthermore, Ohgami et al. reported on endoscopic thyroidectomy using the pectoral approach [16], while Yamashita et al. reported a procedure for endoscopic thyroidectomy via the submandibular approach [17].

We herein reported the use of the EZ-VANS method for endoscopic thyroidectomy. In this method, a Lap-protector mini was inserted into a small axillary incision and the E·Z-access was fitted. After that, multiple E·Z-ports were placed for the videoscope, suction, Harmonic scalpel, and forceps. These instruments were developed for single-port laparoscopic abdominal surgery [18]; however, we have applied them to endoscopic thyroidectomy. We chose a 9 cm E·Z-port for the Harmonic scalpel and forceps because it could traverse the clavicle and reach the lower pole of the thyroid, making it easy to insert the forceps and Harmonic scalpel into the cervical working space. On the other hand, we used a 5 cm short port for the flexible videoscope to achieve a clear view of the working space from multiple angles.

With the anterior chest wall approach that was reported by Shimizu et al., the thyroid was approached from the lateral aspect and the distance from the wound to target was shorter than with the axillary approach. Accordingly, the surgeon could treat both the upper and lower poles of the thyroid easily and it was also easy to find the parathyroid gland and the recurrent laryngeal nerve [9, 10]. On the other hand, the cosmetic outcome was better with the axillary approach than with the cervical or anterior chest wall approaches because the scar was hidden unless the arm was abducted [14]. We performed endoscopic thyroid surgery in 30 patients from January 2007 to January 2010 using the anterior chest wall approach [9, 10] while gradually moving the wound to the axilla. From February 2010 to September 2014, we performed endoscopic thyroidectomy using the EZ-VANS method via the axillary approach, which was carried out in 37 patients.

In the VANS method, the thyroid gland is approached between the SCM and the lateral border of the sternohyoid (SH) muscle [9, 10]. This method was difficult for the axillary approach because the surgeon had to overcome three obstacles to reach the working space: (1). the surgical devices must negotiate the long and narrow space from the axilla to the clavicle, (2) the devices must pass the clavicle, and (3) the SH muscle must be mobilized to expose the thyroid. With the use of the EZ-VANS method, the SCM was detached between the head of the sternum and clavicle, the lateral border of the SHM was easily exposed and the thyroid could be approached from the axillary incision via a straight route.

In EZ-VANS, the gasless method was adopted to maintain the working space. When CO2 gas was used, smoke due to the electrocautery or the Harmonic scalpel obstructs the view of the surgeon almost immediately, because the working space for endoscopic thyroidectomy is so small, and the operating field is also easily constricted during the suction of blood and fumes [19]. On the other hand, the gasless method with retraction of the cervical skin creates a working space that does not shrink or become constricted during the suction of blood and fumes. The gasless method also has no risk of complications such as hypercapnia, respiratory acidosis, tachycardia, subcutaneous emphysema, and air embolism. Moreover, in the gasless endoscopic method, some parts of the operation can be performed under direct vision, and instruments designed for open surgery may also be used [20]. We retracted the cervical skin together with the SHM, as mentioned above, and performed gasless surgery. The E·Z-access was easy to attach and remove; thus, it allowed a quick response if smoke and bleeding obscured the surgeon’s vision in the small working space.

Frequent collision of the instruments may often occur when the instruments are inserted through the E·Z-port and manipulated in the long and narrow access route [21]. Recently, this challenge was partially overcome by modifying the E·Z-access from a round port to an oval port (Fig. 1). The aim of widening the E·Z-port was to reduce the frequency of instrument collision. This problem could also be overcome by setting another 5 mm port at the edge of the neck for the endoscope, which enabled multi-angular viewing [22].

Currently, robotic endoscopic thyroidectomy using the da Vinci® Surgical System (Intuitive Surgical Inc., Sunnyvale, California, USA) has been demonstrated to achieve good results [3–5]. Robotic thyroidectomy has several advantages. The imaging system consists of two cameras that can produce binocular 3-D vision. The use of an EndoWrist with a total of seven degrees of freedom, and scaled and tremor-filtered movement, increases the flexibility of the operative procedures, translates all of the surgeon’s motions into precise movements of the robotic arms, and exceeds the limits of human wrist function. The fulcrum of the robot arm is fixed to the edge of the wound to allow the EndoWrist to be operated more smoothly and safely in the small working space. When endoscopic thyroidectomy is performed using the EZ-VANS method, surgical instruments are inserted through the E·Z-port, which is fixed with the E·Z-access, and the surgeon can manipulate these instruments smoothly and stably similarly to robotic surgery. Lee et al. reported that robotic surgery had benefits for young surgeons who are learning endoscopic thyroid procedures, because the learning curve for hand skill acquisition in robotic surgery was shown to be more favorable than that for normal endoscopic thyroidectomy [5]. It was also suggested that the EZ-VANS method had the same benefit for learning the skills of endoscopic thyroidectomy as easily as with open thyroidectomy.

Recently, endoscopic surgical techniques have generally been accepted as cosmetically advantageous methods for managing benign tumors, follicular adenoma, and adenomatous hyperplasia [10–12]. However, whether these methods should be applied to malignant tumors is still debatable. Both the radicality and safety of surgery are necessary to prevent local recurrence and distant metastasis. In this context, the safety and radicality of endoscopic operations for malignant tumors of other organs have been confirmed [23]. For instance, it has been previously reported that there were no differences in the recurrence rate and survival rate between laparotomy and laparoscopic surgery, while endoscopic surgery achieved a better cosmetic outcome and QOL in comparison with open surgery. There have been several reports regarding the endoscopic surgical results for papillary thyroid microcarcinoma in low risk patients [24, 25]. Miccoli et al. showed that there was no difference between conventional open thyroidectomy and endoscopic thyroidectomy with regard to the completeness of resection as demonstrated by the 24-h 131I uptake on thyroid scans and postoperative thyroglobulin levels [24]. Lombardi et al. reported on the safety and effectiveness of endoscopic thyroidectomy and selective cervical lymph node dissection in low risk patients with papillary thyroid microcarcinoma [25]. In the present series, we performed 14 endoscopic thyroidectomies using the EZ-VANS method for malignant tumors, and there was no local recurrence or distant metastasis. It was difficult to make a decision regarding the safety and prognosis of endoscopic thyroidectomy because the observation period was short; therefore, careful follow-up will be necessary. When the safety and curability of laparoscopic resection are confirmed for various thyroid diseases in the future, the indications for such operations will be gradually expanded.

Conclusion

Endoscopic thyroidectomy is a valuable treatment method for patients with benign thyroid tumors. It can also be selectively applied as an effective treatment modality for patients with early thyroid cancer, such as papillary thyroid microcarcinoma. Moreover, the EZ-VANS system is useful for the smooth acquisition of the skills required to perform endoscopic thyroid surgery.