Robotic-assisted thymectomy for locally advanced thymic malignancy: technical refinement and oncologic outcomes from a 20-year cohort

Introduction

Thymic epithelial tumors (TETs), although rare (age-adjusted incidence 0.13/100,000 person-years), constitute 50% of anterior mediastinal tumors in adults (1). Radical resection (R0) is the cornerstone of treatment, which significantly influences disease-free and overall survival (2). The recurrence rate is as low as 6% for early staged patients; however, advanced-stage [tumor-node-metastasis (TNM) II–IV] thymic malignancy demonstrate substantially higher recurrence rates (26–36%) (3), underscoring the critical need for optimized surgical approaches.

Thymectomy can be performed through different surgical modalities, from conventional sternotomy to less invasive methods such as video-assisted thoracoscopic surgery (VATS) and robotic-assisted thymectomy (r-ThX), as well as subxiphoid thoracoscopic surgery and transcervical approach (4-9). Although minimally invasive surgery including robotic surgery has revolutionized early-stage thymoma management and had been recommended as one of the standard of cares for early staged thymoma (2,10-12), evidence supporting its use in advanced disease (TNM II–IV) settings remains limited and faces unresolved challenges: ambiguous selection criteria for minimally invasive approaches, variable conversion rates (15–40% across studies) (13,14), and lack of objective intraoperative decision-making protocols. Many studies have combined r-ThX with VATS under the umbrella of minimally invasive approaches or have included only a small number of advanced cases alongside early-stage ones (15-17). Recently, Gu et al. (18) reported their experience of VATS and demonstrated its noninferiority compared to median sternotomy for T2–3 stage thymic malignancies in terms of oncologic outcomes, with similar 5-year recurrence rates (78.2% vs. 78.5%), and a lower post-operative complication rate and a faster recovery process. r-ThX has been reported to offer safety and feasibility comparable to, if not exceeding, that of other approaches for early-stage thymic malignancies (19,20). However, its use in the advanced-stage disease setting has not been sufficiently studied. This highlights critical gaps that our study aimed to address: the feasibility of r-ThX in locally advanced cases including confounding with unexpected T4 disease, preoperative prediction of vascular adhesion complexity, and intraoperative decision thresholds for conversion. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1668/rc).

Methods

Study design and data source

This study included all consecutive cases who underwent thymectomy for thymoma or thymic carcinoma (TC) between January 2003 and January 2024 in Charité-Universitätsmedizin Berlin. Patients who underwent initial thymectomy and with pathologically confirmed stage II/III/IV (9th TNM) (21) thymoma or TC were included, and those who only underwent exploratory biopsy or underwent repeated surgery after recurrence were excluded. Those who received planned video-assisted exploratory or adhesion dissection and transfer to sternotomy were deemed as sternotomy. The patient flow, including inclusion and exclusion criteria, is illustrated in Figure S1. Perioperative data was collected from the hospital information system and the follow-up data recorded during outpatient visits or from a telephone interview. The clinical details collected included perioperative treatment and surgical method, post-operative complications, and pathological reports including tumor size, stage, and resection margins.

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The Charité-Universitätsmedizin Berlin Institutional Review Board provided written approval for this study (IRB: EA1/025/11). Based on its retrospective method, the informed consent process was waived.

Process of diagnosis and preoperative patient selection criteria

Preoperative diagnosis was made according to the typical features (e.g., lobulated and homogenous/slightly heterogeneous mass) of computed tomography (CT) and/or magnetic resonance imaging (MRI) (22). For those thymic tumors diagnosed as local advanced and initially considered unresectable or potentially resectable, an additional positron emission tomography (PET)-CT was conducted to exclude the potential metastasis, and a multimodality strategy was recommended after a multidisciplinary team (MDT) discussion. Patients with R0 resectable potential were scheduled for radical thymectomy.

The decision between r-ThX and sternotomy was based on comprehensive preoperative assessment including: CT/MRI assessment of tumor-vessel relationship: a >50-degree encasement of the pulmonary artery or aorta, or >30-degree superior vena cava (SVC) or left brachiocephalic vein, and disappearance of the fat layer (23); assessment of other organ involvement: extensive pericardial involvement requiring reconstruction, hilar invasion, phrenic nerve involvement; tumor size and location assessment; patient factors: BMI, comorbidities, previous thoracic surgery.

Primary sternotomy candidates: extensive vascular involvement, hilar invasion.

Primary r-ThX candidates: limited vascular involvement, unilateral phrenic nerve involvement, limited pericardial involvement.

The operation process

All operations aimed to achieve complete thymectomy including resection of the tumor, thymus, all anterior mediastinal fat, peri-thymic lymph nodes, and enlarged nodes encountered during dissection at the para-aortic, low anterior cervical, and supradiaphragmatic regions, we conduct an en-bloc resection with involved structures as the standard to avoid tumor dissemination.

Generally, the median sternotomy approach remained our priority choice for cases with extensive vascular involvement, consistent with the conventional surgical standard (24,25). For r-ThX, we utilized our traditional left-sided approach with three robotic arms and one assistance port, unless the tumor predominantly occupied the right hemithorax; the technical details and the benefit of this left-sided approach have been described before (26,27).

Our surgical approach adhered to a standardized protocol that included specific decision points for conversion as needed (Figure 1).

• Initial assessment: following port placement and CO₂ insufflation (8–10 mmHg), we systematically evaluated the tumor-vessel relationship and extent of local invasion.
• With the help of the robotic camera’s magnification and 3D visualization on intra-operative assessment, a conversion to sternotomy was always prepared when encountered absence of perivascular fat plane and difficulty in blunt dissection, tumor tissue directly adherent to vessel wall even after dissection of the fibral membrane, or major bleeding unmanageable by surgical team. For rare cases, limited left brachiocephalic vein involvement was partially resected robotically through subxiphoid fourth trocar with stapler, and for all other major vascular involvement, planned conversion was performed.
• Other localized invasion management: for limited pericardium invasion, robotic pericardial resection was performed, and for extensive pericardial involvement requiring reconstruction, conversion was considered, but robotic patch implantation may be performed in most cases. For phrenic nerve adherence with preoperative diaphragm motion, we attempted careful neurolysis, and if nerve sacrifice was necessary, we ensured unilateral involvement only. For lung invasion, wedge resection was performed; for hilar invasion, we converted to a conventional open approach.

Figure 1 Decision tree for surgical approach selection and conditions for conversion during the surgery. CT, computed tomography; Intra-op, intra-operative; LBCV, left brachiocephalic vein; MDT, multidisciplinary team; MG, myasthenia gravis; MRI, magnetic resonance imaging; PA, pulmonary artery; PET, positron emission tomography; Postop, post-operation; r-ThX, robotic-assisted thymectomy; SVC, superior vena cava; TNM, tumor-node-metastasis.

When encountering unexpected tight adhesions that might lead to incomplete resection, surgical clips were placed at resection margins. The specimen was retrieved intact through an endo bag to prevent seeding.

All patients were monitored in the intensive care unit (ICU) before returning to the general ward after stabilization. Complications occurring after surgery were classified using the Clavien-Dindo system during hospitalization or within 30 days after surgery, whichever was longer (28).

Staging and follow-up

The World Health Organization (WHO) classification system was utilized to categorize the histologic subtypes of tumors into categories A, AB, B1, B2, B3, or C (29). The Masaoka-Koga and 9th TNM staging system systems were employed (3,30). Operative notes and pathologic reports were meticulously reviewed to determine whether R0, R1, or R2 resection was achieved. Specifically: R0 indicates complete resection with negative margins; R1 denotes microscopic positive resection; R2 signifies macroscopic positive resection.

Postoperative multimodality treatment, including postoperative radiotherapy (PORT) and adjuvant chemotherapy, was determined by the MDT. For instance, if a non-R0 resection was decided upon or the WHO stage was classified as B2/B3, PORT was recommended.

Patients were advised to undergo follow-up with contrast-enhanced CT of the chest every 6 months until 3 years, and then annually until 10 years. The primary endpoints included time to recurrence and death, calculated from the date of operation. Secondary endpoints included perioperative safety, including complications and deaths. Recurrence was defined as a newly diagnosed neoplasm identified through contrast-enhanced CT, confirmed by pathological evidence (needle biopsy or surgical specimen), or a clinical diagnosis made by the surgeon.

Statistical analysis

Statistical analyses were performed using R software (version 4.4.2, R Foundation for Statistical Computing, Vienna, Austria). The characteristics and clinical outcomes of patients in the r-ThX group were compared to those in the open thymectomy (OT) group. Continuous variables were summarized as medians with ranges and analyzed using the Mann-Whitney U test to assess differences between groups. Categorical variables were summarized as proportions and analyzed using Fisher’s exact test to evaluate associations. The primary oncological outcomes, including R0 resection rates, recurrence, and mortality, were described for both groups. The significance level of P<0.05 was considered statistically significant.

Survival analyses were not powered for adjusted inference due to baseline imbalance and low event counts; exploratory Kaplan-Meier curves and Cox regression analysis are provided in the supplementary file (Figure S1 and Table S1) without inferential comparison.

We also performed a post-hoc analysis to address the potential learning curve effect.

Results

Between January 2003 and January 2024, 41 patients with advanced thymoma or TC underwent thymectomy at our center, meeting the study’s inclusion criteria (r-ThX: 20, sternotomy: 21). The patients were divided into the r-ThX group and the sternotomy group. There were more male patients (55% vs. 71%) in both groups, and the median ages at operation were 49 and 59 years, respectively. More patients were concomitant with myasthenia gravis (MG) in the r-ThX group (70% vs. 9.5%). Notably, the tumor burden in the sternotomy group was significantly higher, with larger tumor (median diameter of the tumor: 8.0 vs. 5.3 cm, P=0.03), higher Masaoka-Koga stage (P=0.006), and higher TNM stage (P=0.006). More neoadjuvant chemotherapy was conducted in the sternotomy group (66.7% vs. 10%, P<0.001). The demographics are shown in Table 1.

The mean operation duration was significantly longer for the r-ThX group (294 vs. 201 minutes, P=0.009), whereas the sternotomy group experienced a slightly longer drainage duration (5.1 vs. 4.5 days, P=0.80). In the r-ThX group, three patients required conversion to sternotomy. Among them, one necessitated an additional right-sided thoracotomy to complete the lobectomy, whereas the other two were converted to sternotomy due to intraoperative major vessel invasion, including one case following minor bleeding from the left brachiocephalic vein. The characteristics of patients who underwent a conversion are provided in Table S2. R1 resection was more prevalent in the sternotomy group (55% vs. 32%, P=0.14). No significant differences were observed in the rates of PORT or postoperative chemotherapy (POChT). The incidence of grade 2 or higher perioperative complications was lower in the r-ThX group (20% vs. 42.9%, P=0.12). Two grade III complications were noted in the r-ThX group. The first involved a patient with a challenging thymoma who was converted from r-ThX to sternotomy, undergoing an R0 resection that included partial resection of the pericardium, a wedge resection of the left upper lung lobe, and partial resection of the left phrenic nerve. The recovery was complicated by pleural effusion and pulmonary infection, leading to a myasthenic crisis, which required tracheal re-intubation for respiratory support. The second case involved phrenic nerve invasion necessitating unilateral phrenic nerve resection, with postoperative respiratory insufficiency requiring re-intubation. The detailed clinical outcomes for both r-ThX and sternotomy groups are summarized in Table 2.

Learning curve analysis showed that the conversion rate decreased from 20% (2/10) in the early period to 10% (1/10) in the recent period. The mean operation time also decreased from 320 to 273 minutes. The characteristics and the clinical outcome were detailed in Tables S3,S4.

The median follow-up duration for the r-ThX group and the sternotomy group was 34.4 (1.1–182.1) and 29.3 (1.0, 95.8) months, respectively. In the r-ThX group, three patients experienced recurrence, and no death occurred, resulting in a progression-free survival (PFS) of 85% (17/20). The time to recurrence for these patients was 6.4, 33.9, and 65.5 months, respectively. In the r-ThX group, 8 patients experienced recurrences and 1 non-oncologic death occurred due to acute cardiac disease, resulting in a PFS of 57.1%. Details of the recurrences and deaths are provided in Table S5.

Discussion

Although MIT has been widely adopted for the management of early-stage thymic tumors, its role in advanced thymic malignancies remains less defined. The advancements of equipment and clinical expertise in our center have facilitated the transition from sternotomy to VATS, and then to r-ThX, and the lesson learned from the transition process underscored the importance of a clear patient’s feasibility and conversion from minimally invasive thymectomy (MIT) to open surgery criteria. During this study, we included 41 consecutively locally invasive thymic tumors cases conducted with r-ThX or sternotomy, given the imbalance in tumor burden and neoadjuvant therapy between groups, we limited our analysis to descriptive statistics and focused on the feasibility and safety of rThX in demanding cases. We provided descriptive Kaplan-Meier curves and Cox analyses in the supplementary file (Figure S2, Table S1), which were not intended for comparative inference. Despite the high tumor burden, there were no perioperative deaths, and at midterm follow-up most patients were disease-free, and all were alive.

The largest series comparing the OT and MIT of 1,223 Masaoka-Koga stage I–III thymectomy registries in the National Cancer Data Base was conducted by Yang et al. (14), which concluded the MIT was associated with shorter length of stay and was not associated with reduced overall survival when compared with OT; however, the number of included stage III cases was limited (n=20), and detailed analysis was not reported. Another study by Gu et al. demonstrated that VATS could achieve superior perioperative outcomes and comparable oncological results to sternotomy in selected advanced TETs, they further proposed a resection index to assess the resectability of the advanced thymic tumor, categorized the vessel invasion as 3 points, and other invasion as 1 or 2 points (18). We appreciate its significance to serve as a reference to patient selection on MIT or sternotomy, and the invasion to the major vessels as the single high-risk index was consistent with our experience. In our r-ThX series, 85% (17/20) cases underwent additional resection including lung (11 cases), pericardium (8 cases), phrenic nerve (3 cases), and major vessel (3 left brachiocephalic vein cases), pleura (1 case).

Another critical factor which was not adequately emphasized was the clear decision path of conversion. One of the reasons for the sometimes-unavoidable conversion is that preoperative imaging may underestimate or overlook invasions to critical structures such as the pleura, phrenic nerve, lung, and major vessels. Gu et al. (18) reported a conversion rate of 13.8%, of which most cases were due to large tumors, except for unexpected bleeding. Our r-ThX series had a similar 15% (3/20) conversion rate, but with different conversion reasons, none of them were because of the tumor diameter, and only 1 conversion was due to hemorrhage of the brachiocephalic vein. The other 2 cases were due to underestimation of preoperative imaging.

In this study, we proposed a structured surgical decision-making map, which includes the choice of upfront r-ThX/sternotomy, or a thoracoscopic exploration before the main procedure, and step-by-step conversion decision tips during r-ThX (Figure 1). Conversion to OT is a strategic decision, not a failure, ensuring safety and oncological integrity. There are several critical questions to be taken into consideration.

For patients comorbid with MG, adequate medication is important before the surgical intervention and during the perioperative period. MIT was reported as having special advantages in reducing the risk of MG crisis (31). Our r-ThX series was consistent with it, with 70% of patients comorbid with MG, and only 1 of them who converted to sternotomy developed a pulmonary infection-induced MG crisis.

For patients with massive invasion and accepted biopsy, the histological types of B2/B3/C have more invasive biological behavior (32), and especially for those confirmed as TC, increased metastasis risk should be taken into consideration, and neoadjuvant therapy should be more proactive for these patients.

When attempting r-ThX on advanced thymic tumors, the experience of the surgeon should be taken into consideration. The learning curve for performing a robotic thymectomy is described as 15–20 cases (33). However, for these challenging cases, we recommend a conservative requirement of the accomplishment of 30+ robotic assisted extended thymectomy for MG or early staged thymoma, and adequate traditional sternotomy experience. In our cohort’s early period (pre-2018), two cases with pericardial and pulmonary parenchymal invasion underwent sternotomy; using today’s criteria, both would likely be candidates for r‑ThX.

In review of the CT scan, tumor size of thymic malignancy was reported to be an important prognostic factor for overall survival (34), but the size itself is not a limitation to adopt the r-ThX. We recently reported our findings on the feasibility and comparable oncological outcome of r-ThX with a 4-trocar technique on early-stage large thymoma (diameters larger than 5 cm) (27); another multicenter study also showed good safety and effectivity of r-Thx in large thymoma (35).

The management of vascular invasion represents the most critical aspect of advanced thymic malignancy surgery. Our experience highlights several key principles: CT/MRI imaging provides initial assessment but may underestimate invasion extent, multidisciplinary team discussion is essential for optimal patient selection for r-ThX, and intraoperative flexibility is necessary. When intraoperative signs of vascular invasion are identified during r-ThX, conversion to sternotomy is generally recommended to ensure complete resection and minimize complications. Only selected cases with limited involvement of the left brachiocephalic vein may be managed robotically with partial resection. Our 15% conversion rate reflects appropriate patient selection, and no major vascular complications occurred under these strict criteria.

The pericardium is frequently involved in thymomas, necessitating pericardiectomy (36). Although minor invasions are manageable with r-ThX, significant defects, particularly laterally, require reconstruction to prevent cardiac herniation (37). Such reconstructions are time-intensive with r-ThX, and conversion to sternotomy should be considered based on the surgeon’s experience and patient condition.

Phrenic nerve involvement is another consideration. If preoperative assessments indicate normal diaphragm motion, nerve preservation during r-ThX is feasible, reducing perioperative complications, especially in MG cases, without compromising oncological outcomes (38).

Pleural invasion is common, with 70.8% of our patients undergoing partial lung resection. Under CO₂ insufflation, thorough ipsilateral pleural exploration can be safely accomplished via robotic-assisted surgery prior to opening the contralateral pleura. Wedge resection suffices for visceral pleura involvement, but hilar invasion necessitates anterior thoracotomy for safety.

Our findings reinforce the role of r-ThX in the management of thymic malignancy; even in selected advanced disease settings, the radical resection and perioperative safety should be the foremost consideration, regardless of the approach. However, our study has several limitations. The rarity of the disease limits our sample size, precluding extensive multivariable analysis, and the imbalanced tumor burden between the r-ThX and the sternotomy prevented the direct comparison between these two approaches. Additionally, the relatively short follow-up duration may not be sufficient to capture late recurrences or long-term outcomes, particularly for advanced thymic malignancies which may have delayed recurrence patterns. Multicenter studies with longer follow-up periods are required to further validate our findings.

Conclusions

r-ThX presents a viable alternative to sternotomy for patients with locally advanced thymic malignancies, particularly in cases involving partial invasion of the pericardium, pleura, and phrenic nerve. Conversion to open surgery remains essential when major vessel invasion is encountered, ensuring patient’s safety and optimal oncologic results. Future multicenter studies are needed to validate these findings and refine surgical decision-making protocols.

Acknowledgments

We would like to acknowledge Liangfeng Zou for providing valuable technical support during the statistical R coding process. We also thank John Snyder and Reese Liu for their assistance with the language editing and figure drawing.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1668/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1668/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1668/prf

Funding: This work was supported by Henan Province Medical Science and Technology Key Research and Joint Construction Project (No. LHGJ20220284 to F.L.).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1668/coif). F.L. reports funding support from the Henan Province Medical Science and Technology Key Research and Joint Construction Project (No. LHGJ20220284). A.M. received speaker or consultancy honoraria or financial research support (paid to his institution) from Alexion Pharmaceuticals, Amgen, Argenx, Axunio, Desitin, Grifols, Hormosan Pharma, Johnson & Johnson, Merck, Novartis, Octapharma, Sanofi, and UCB and serves as a member of the Medical Advisory Board of the German MG Society. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Charité-Universitätsmedizin Berlin Institutional Review Board (IRB: EA1/025/11) and the requirement for individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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(English Language Editor: J. Jones)