Thymomas are rare intrathoracic neoplasms of the thymus, with an annual incidence of approximately 0.15 per 100,000 person-years [1]. Surgical intervention, still the only curative treatment, traditionally is performed through a median sternotomy, with complete resection of the tumor, thymus, thymic cervical extensions, and surrounding perithymic fat [2, 3]. With the advent of improved optics and computer-assisted surgical systems, minimally invasive thymectomies by video-assisted or robotic techniques are becoming increasingly popular [4].

We present our operative method of thymectomy via unilateral robot-assisted thoracoscopic surgery (RATS) for the treatment of Masaoka stages 1 and 2 thymoma without myasthenia gravis. We compared the short-term outcomes between patients undergoing our procedure and those undergoing transsternal thymectomy (TST).

Patients and methods

Between January 2009 and December 2012, 584 patients presented with primary thymic tumors, which were resected with curative intent. Of these 584 patients, 74 (32 men and 42 women) with a pathologic diagnosis of Masaoka stages 1 and 2 thymoma with no myasthenia gravis who underwent RATS or TST were selected for the study.

The use of RATS and TST with curative intent was approved by our local ethics committee, and informed consent was obtained from all the patients. All participants provided their written informed consent to participate in this study, and the ethics committee of our hospital approved this consent procedure. Of the 74 patients, 23 underwent thymoma resection using RATS, and the remaining 51 underwent TST.

In each case, the anterior mediastinal tumor, histologically confirmed as thymoma after surgery, demonstrated features highly suggestive of thymoma without signs of invasion to the surrounding structures, as demonstrated by computed tomography (CT) before surgery. The RATS or TST procedure was indicated for a thymoma smaller than 5 cm.

For RATS, all the patients were anesthetized using a double-lumen tube for split-lung ventilation and placed left or right side up at 30°. The first incision generally was performed in the fifth intercostal space at the anterior axillary line. Thus, the camera was inserted to explore the chest cavity, and carbon dioxide (CO2) was inflated at 4–8 mmHg to enlarge the operating space for safe performance of the other port incisions placed at the anterior axillary line, at the third intercostal space, at the fifth intercostal space, and at the midclavicular line.

The right arm had a spatula (EndoWrist; Intuitive Surgical, Sunnyvale, CA, USA) with an ultrasonically activated function to perform dissection, whereas the left arm had a Cadiere forceps (EndoWrist; Intuitive Surgical), an atraumatic instrument for grasping the normal thymus. The 30° scope permitted excellent visualization of normal thymic tissue and the thymoma’s capsule. The normal thymic tissue and the perithymic fat were used for grasping and for traction of the tumor, avoiding direct manipulation of the tumor to minimize the risk of capsule damage.

After inspection of the thymus gland and individuation of the thymoma, the dissection generally started inferiorly, first from the pericardiophrenic angle. It then continued on to the retrosternal area, finding the right or left mediastinal pleura and the phrenic nerve and thus permitting safe dissection of the right or left inferior horn under direct vision of the nerve. Consequently, the dissection continued upward to the neck until the superior horns were identified. The thymic veins were divided with an ultrasonically activated device.

The lesions were removed with endoscopic pouches from the cavity through the port incision in the midaxillary region. If necessary, the incision was enlarged (to a 3-cm maximum). No additional utility incision was used. A drainage tube was inserted, generally 32Ch. All the thymic and perithymic fat was dissected according to the Masaoka criteria [5], and the completeness of the thymectomy was assessed by macroscopic inspection of the thymic bed and specimen.

The transsternal thymectomies were performed by several different surgeons. Patients were positioned in the supine position with the arms either tucked in at their sides or slightly extended at the side. All the patients were ventilated with a single-lumen endotracheal tube. Either a complete or partial sternotomy was used, and the thymus and thymic pathology were resected en bloc. All the thymic and perithymic fat was dissected according to the Masaoka criteria [5], and the completeness of the thymectomy was assessed by macroscopic inspection of the thymic bed and specimen.

We evaluated the duration of surgery, the amount of intraoperative blood loss, the duration of chest drainage, the duration of the postoperative hospital stay, and the postoperative complications. The diagnoses of all resected thymomas, the surgical margins, and the Masaoka stage were confirmed by histologic examination. The size, shown by the maximal diameter of the tumor in the resected specimen, was measured. Recurrence of thymoma was evaluated by CT of the chest 6 and 12 months after surgery, then once yearly thereafter.

The data are reported as means ± standard deviations. Statistical analysis was performed with SPSS 16.0 statistical software (SPSS Inc., Chicago, IL, USA). Probability values were generated with the Chi square test (for categorical data) and the unpaired t test (for noncategorical data). A p value lower than 0.05 was considered statistically significant.

Results

The preoperative characteristics of the two groups of patients are shown in Table 1. The RATS group comprised 11 men and 12 women with a mean age of 52.5 years. The TST group included 31 men and 20 women with a mean age of 50.1 years. In the RATS group, 15 patients were approached from the right thoracic cavity and 8 patients from the left thoracic cavity.

Table 1 Characteristics of the patients in the RATS and TST groups
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The surgical outcomes in the RATS and TST groups are shown in Table 2. The duration of surgery and the intraoperative blood loss were significantly less (61.3 ± 21.8 vs. 466.1 ± 91.4) and the postoperative hospital stay significantly shorter days in the RATS group than in the TST group (3.7 ± 1.1 vs. 11.6 ± 10.4 days) (p < 0.01).

Table 2 Surgical outcomes of the patients in the robot-assisted thoracoscopic surgery (RATS) and transsternal thymectomy (TST) groups
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The da Vinci system enables the surgeon also to dissect the left thymic lobe accurately from a right-sided access in most patients. No patients in the RATS group underwent conversion to open surgery. No surgical complications (e.g., massive bleeding) were observed in this series except for one case of pulmonary atelectasis, which appeared in a male patient 2 days after surgery. Alternatively, no surgical complications (e.g., massive bleeding) were observed in the TST group except for one case of pneumonia and one case of pleural effusion that occurred postoperatively.

In both groups, the surgical margins were free of tumors. No recurrence was observed during the postoperative follow-up period of 16.9 months (range, 1–48 months) in the RATS group and 18.1 months (range, 1–48 months) in the TST group.

Discussion

The open surgical approach generally was accepted as a gold standard for resection of thymoma [6–9]. However, during the last decades, both thoracoscopic and, more recently, robotic approaches have been introduced into the thoracic field and also applied for thymectomy. Several published data regarding minimally invasive thymectomy have shown interesting outcomes, with an emphasis on less operative trauma, shorter hospital stay, preserved pulmonary function, and better cosmetic results [10–13].

With introduction of the da Vinci Surgical System, surgeons gained a versatile and ideal option for endoscopic resections in thoracic surgery. The outstanding visibility afforded by a robot-assisted system is due to its three-dimensional magnified view of the operating field and the dexterity of the instruments that facilitate surgery with spectacular precision and security in contrast to open transsternal thymectomy [14–16].

In addition, RATS has proved its advantages in surgical procedures, mainly a shorter hospital stay and less blood loss [17]. However, only a few major series have reported the surgical results of RATS surgery for thymoma. In the surgical treatment of noninvasive thymoma, the choice of RATS and TST still are controversial.

Our short-term surgical outcomes showed the safety and efficacy of RATS for Masaoka stages 1 and 2 thymoma. The RATS approach has shown benefits and advantages in terms of less invasiveness, decreased blood loss, shorter duration of surgery, and reduced hospital stay compared with traditional surgery. Furthermore, no serious postoperative complications occurred in the RATS group. In addition, no case was converted to open surgery, and no case required blood transfusion. Although the follow-up period was short, no patient experienced recurrence of thymoma.

Our results suggest that RATS thymectomy is tolerated for early-stage thymoma. Intraoperative blood loss was significantly less in the RATS groups (61.3 ml) than in the TST group (466.1 ml) (p < 0.01).

An important point is that we use ultrasonic devices in RATS. Great care must be taken to avoid vascular and nervous injuries. Bleeding, the most serious complication, should be kept in mind during this operation. Special attention must be paid because venous drainage of the gland to the innominate vein involves thin vessels. Each must be isolated and coagulated, then cut with the ultrasonic device without clipping so as to minimize the amount of bleeding.

In the RATS series, no patients experienced conversion to an open procedure. Although it is small, the da Vinci tool is excellent in terms of handling and indispensable for this operating method.

Additionally, another important criticism concerned the surgical approach for patients with thymoma. In the past, many surgeons hesitated to perform RATS resection of thymomas, and median sternotomy generally was accepted as a gold standard. However, in 2012, a comparative study conducted by Weksler et al. [13] with 50 patients showed that RATS thymectomy for early-stage thymoma provides better surgical outcomes than open surgery.

In our small series, even with its short follow-up period, we observed no local or pleural recurrence. We believe that the robotic system facilitates the individuation of the thymoma capsule and normal thymic tissue and allows safe manipulation. Nevertheless, an important factor that affected the success of the minimally invasive approach probably was the dimension of the lesion. In our series, the mean thymoma dimension was 29.6 ± 7.7 mm in RATS and 32.6 ± 6.7 mm in TST, similar to the dimensions reported in the studies for the video-assisted thoracoscopic surgery approach [18]. However, the indolent nature of thymomatous disease requires a long follow-up period [19] of 10 years for evaluation of survival and the disease-free rate. Thus, further multi-institutional studies with larger series are necessary.

Because the high costs are one of the main points of criticism voiced in connection with robot-assisted operations, we evaluated the hospitalization costs of thymectomy for various minimally invasive approaches. Use of the robot is more expensive. We demonstrated higher costs than for conventional TST, with no difference in the statistics report. These high costs are caused primarily by the expensive robotic instruments, which can be reused only a limited number of times [20].

The current study had some limitations, including its retrospective nature, which may have resulted in a selection bias. Moreover, the study sample was small, with a short follow-up period. However, this was an initial experience resulting from gained skill in robotic surgery for thymoma, and the main aim was to compare perioperative outcomes for patients who underwent transsternal or robot-assisted thymectomy and to analyze the safety and technical feasibility of the robotic approach for early-stage thymomas. In fact, few data regarding the robotic approach focused on thymoma have been published, and our small series is the largest one to our knowledge.

Conclusion

This preliminary study demonstrates the safety and feasibility of robotic thymectomy for thymoma, with no mortality, low morbidity, and no nerve or vessel injury. Nevertheless, it is hoped that randomized multi-institutional trials with long follow-up periods will be designed to compare the transsternal and robotic approaches and to evaluate the oncologic outcomes.