Treatment approaches and outcomes of major chest wall resections and reconstructions in patients with soft tissue and bone sarcomas: a retrospective observational study

Introduction

Background

Soft tissue sarcomas (STSs) and bone sarcomas (osteosarcoma, Ewing sarcoma, and chondrosarcoma) are extremely rare malignancies, each representing less than 1% of all malignancies of the adult population (1). According to the latest World Health Organization classification, STSs comprise over 100 different subtypes (2).

Rationale and knowledge gap

Recent studies have demonstrated the benefits of treating patients with sarcomas through multidisciplinary teams in experienced sarcoma centers (3-5). The primary goal of surgery with curative intent is microscopically negative (R0) resection. En bloc radical resection remains essential for the prognosis of patients with localized disease (6). However, in patients with chest wall sarcomas, surgical treatment poses a considerable challenge as these tumors often require extensive resection and complex reconstruction (7,8).

Objective

In this study, we aimed to analyze the surgical approaches, focusing on the extent of resection and type of reconstruction, and oncological outcomes of patients with chest wall sarcomas treated at our center, and to identify factors that influence patient prognosis and long-term survival. This analysis is crucial to understand the effectiveness of current surgical approaches. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-472/rc).

Methods

Ethical statement

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and approved by the Ethics Committee for Multi-Centric Clinical Trials of the Motol University Hospital (Ref. EK-189/20). The requirement for obtaining informed consent was waived due to the retrospective design.

Study design and population

This was a retrospective, single-center, observational case series. We retrospectively reviewed data of patients who were surgically treated at our sarcoma reference center between May 2014 and February 2022. Patients with deep-seated/subfascial primary or recurrent STSs or bone sarcomas of the chest wall requiring extensive resection and complex reconstruction were included in the analysis. Patients with benign and epithelial tumors, true intrathoracic sarcomas not requiring chest wall resection, superficial tumors, sarcomas of the spine region requiring vertebral resection, metastatic sarcomas from different primary sites, and those who underwent palliative surgery lacking curative intent were excluded. Patients with atypical lipomatous tumor/well-differentiated liposarcoma were also excluded because the standard surgical approach for their treatment was extracapsular extirpation without extensive resection, similar to that for corresponding tumors in the extremities (6).

Primary disease was defined as STS or bone sarcoma initially diagnosed and treated at our center. Recurrent disease was defined as a history of sarcoma diagnosis and surgical treatment at another institution (Table 1, Figure 1). This cohort included patients who either underwent non-radical initial surgery or experienced disease recurrence following the initial treatment at other institutions.

Figure 1 Initial diagnosis and treatment versus operation dates. Identification of each patient’s timeline from initial diagnosis to operation, providing a clear overview of the treatment and follow-up intervals.

Preoperative evaluation

Preoperatively, all patients underwent thoracic imaging using contrast-enhanced computed tomography (CT) and magnetic resonance imaging (MRI). MRI has been established as the standard method for local staging of chest wall sarcomas because it is superior to CT in providing information regarding tumor localization, infiltration of surrounding tissues, relationships to critical structures, intratumoral morphology, presence of satellite lesions, and differentiation between infiltration and postoperative fibrotic changes (9).

Histological confirmation of the sarcoma type was performed through analysis of specimens obtained by ultrasonography- or CT-guided biopsy (for patients with primary disease), or previously obtained surgical specimens (for patients with recurrent disease). All histopathological examinations of both preoperative and postoperative specimens were conducted by an expert sarcoma pathologist. Tumor grading was performed according to the Fédération Nationale des Centres de Lutte Contre le Cancer grading system (10). Definitive specimens from patients who underwent preoperative radiotherapy, chemotherapy, or chemoradiotherapy were not graded.

Patients who were scheduled for extensive resection also underwent preoperative evaluation of lung and heart function through spirometry and spiroergometry, respectively.

According to the histopathological findings, patients were divided into two groups: STS and bone sarcoma. Additionally, in each group, patients were further divided into two subgroups based on their disease status (primary or recurrent).

Treatment

Treatment regimens were determined by a multidisciplinary sarcoma team composed of experienced specialists, ensuring comprehensive and tailored approach to patient care for optimal outcomes. For patients with Ewing sarcoma, the Euro Ewing 2012 protocol was applied (11).

The first step in planning the extent of resection and type of chest wall reconstruction is a precise evaluation of the preoperative MRI scan. In most cases, tumors arising from the ribs or in close proximity to the ribs necessitate resection of the bony structures. Some patients may also require resection of the diaphragm, lungs, or pericardium. If rib resection is performed, the extent is usually one healthy rib/intercostal space above and below the tumor, ensuring radical resection of most histological subtypes. In cases of infiltration of the sternum, partial or complete sternectomy is required (12). Diaphragm reconstruction, when required, is performed by suture or, for larger defects, by monofilament polypropylene mesh. Parenchyma-sparing resection of the lungs is performed when possible; however, anatomical resection is often safer and more convenient. Pericardial resection is followed by reconstructing larger defects using bovine pericardium or the Gore-Tex patch to prevent heart herniation. Special care and preoperative planning must be taken when dealing with certain histological subtypes of infiltrative growth, such as myxofibrosarcoma and undifferentiated pleomorphic sarcoma (13).

In general, in our center, we perform three types of chest wall reconstruction depending on the extent of resection: (I) reconstruction using monofilament polypropylene mesh, combined with a titanium rib bridge in cases of large defects (Figure 2); (II) reconstruction using mostly pedicled latissimus dorsi flap (Figure 3); and (III) combination of both aforementioned methods (Figure 4). The surgical resection was classified as microscopically complete (R0), microscopically incomplete (R1), or macroscopically incomplete (R2) (10).

Figure 2 Reconstruction of the chest wall using monofilament polypropylene mesh, in large defects combined with titanium rib bridge. (A) Resection and reconstruction; (B) preoperative magnetic resonance.

Figure 3 Reconstruction of soft tissues using mostly pedicled latissimus dorsi flap. (A) Resection and reconstruction; (B) preoperative magnetic resonance.

Figure 4 Reconstruction of the chest wall using monofilament polypropylene mesh and pedicled latissimus dorsi flap. (A) Resection of the chest wall; (B) reconstruction using monofilament polypropylene mesh and pedicled latissimus dorsi flap.

All patients received antithrombotic therapy using low-molecular-weight heparin. Prophylactic antibiotic treatment consisted of a single perioperative intravenous dose of broad-spectrum antibiotics. Except for patients with Ewing sarcoma, no neoadjuvant therapy was indicated in our cohort.

Postoperative adverse events were recorded and classified using the Clavien-Dindo classification (14).

Follow-up

Clinical follow-up involved contrast-enhanced CT and thoracic MRI every 6 months for G1 sarcomas and every 3–4 months for G2 and G3 sarcomas over the first 3 years. The frequency of imaging was designed to balance early detection of recurrence or metastasis with patient safety and healthcare resource management. The differences in monitoring schedules for G1, G2, and G3 sarcomas reflected their varying degrees of malignancy and associated risk for recurrence. Subsequent follow-ups included contrast-enhanced CT and thoracic MRI every 6–12 months.

Statistical analysis

Kaplan-Meier’s curves were plotted to analyze the overall survival (OS), metastasis-free survival (MFS), and recurrence-free survival (RFS). OS was defined as the time from surgery to death, MFS as the time from surgery to development of metastases or death, and RFS as the time from surgery to disease recurrence or death. The log-rank test was used to compare the survival outcomes between patients with primary and recurrent STSs.

To identify factors influencing OS, we employed Cox proportional hazards regression analysis to evaluate the prognostic relevance of clinicopathological variables, including age, sex, disease status (primary vs. recurrent), and presence of local recurrence and metastasis.

All statistical analyses and data visualization were performed using GraphPad Prism^® 10.1.2 (GraphPad Software, San Diego, CA, USA). P values equal to or less than 0.05 were considered to indicate statistical significance.

Results

Patient characteristics

Overall, 38 patients were included, 22 in the STS and 16 in the bone sarcoma group. The clinicopathological characteristics of patients in the STS and bone sarcoma groups are shown in Tables 2,3, respectively.

Among the 22 patients in the STS group, 10 (45.5%) were treated for primary tumors and 12 (54.5%) for recurrent tumors (local recurrence or persistence of the tumor initially treated at another institution). The average tumor size in this group was 10.65 cm (range, 5.5–22.5 cm). The most prevalent histological subtype was undifferentiated pleomorphic sarcoma, accounting for 40.00% and 25.00% of tumors in the primary and recurrent subgroups, respectively. Nearly all patients in this group (21/22) were indicated for primary surgical resection or re-resection, except for one patient who underwent primary nonradical resection followed by adjuvant chemotherapy and was subsequently recommended for reoperation.

Of the 16 patients in the bone sarcoma group, 12 (75%) had chondrosarcoma and 4 (25%) had Ewing sarcoma. Among all, 15 (93.75%) patients were treated for primary tumors and only one (6.25%) for recurrent tumor (local recurrence following prior surgery at another institution). The average tumor size in this group was 9.70 cm (range, 2.5–19.0 cm). All surgeries encompassed wide excisions. R0 resection margins were achieved in 21/22 (95.45%) patients in the STS group and 15/16 (93.75%) patients in the bone sarcoma group. In one patient of the bone sarcoma group, multiple lung metastases that were not detected by preoperative staging CT were discovered intraoperatively.

Treatment

Extent of resection and reconstruction techniques

Major soft tissue resection requiring reconstruction with a flap was necessary in 10 patients. Pedicled latissimus dorsi flap alone was used to reconstruct 7 out of 10 defects, while in the remaining 3 cases, we used free latissimus dorsi, bilateral Keystone, and pedicled latissimus dorsi plus Fillet flaps, respectively.

Rib resection was required in 14 patients with STS and all 16 patients with bone sarcoma. In all cases, 1–5 ribs were resected. The distribution of ribs resected in the overall population, indicating the pattern and extent of surgical interventions, is presented in Figure 5.

Figure 5 Patients per resected rib. Column graph showing the number of patients per resected rib. Visualization of the distribution of patients according to which ribs were resected during their surgeries helps in understanding the patterns and extents of surgical interventions for these patients.

Partial sternal resection was performed in 3/22 patients with STS, all with primary tumors, and in 2/16 patients with bone sarcoma. There were no primary sternal tumors, only those expanding to and infiltrating the sternum. In all cases, half of the sternal body was resected with adjacent unilateral ribs and cartilages.

Lung resection was necessary for three patients in the STS and one patient in the bone sarcoma group, and one patient in each group required pericardial resection and reconstruction. Resection and reconstruction of the diaphragm were performed in two and four patients with STS and bone sarcoma, respectively.

Owing to the extent of the disease, one patient with recurrent STS underwent forequarter (interscapulothoracic) amputation.

Postoperative adjuvant therapy

Adjuvant radiotherapy was indicated in 4/22 patients with STS and 2/16 patients with bone sarcoma. In the remaining cases, it was either contraindicated (in patients who had previously undergone radiotherapy for other diseases, making them contraindicated for another reradiation) or not indicated (solitary fibrous tumors, radiation-associated angiosarcoma, early distant metastasis, and prolonged healing). Two patients refused radiotherapy.

Adjuvant/palliative chemotherapy was administered to 2/12 patients with recurrent STS upon early detection of lung metastasis. No patients in the bone sarcoma group underwent adjuvant chemotherapy after radical surgery; however, palliative chemotherapy was indicated following palliative chest wall resection in the patient with intraoperatively discovered lung metastasis.

Complications

Severe complications (Clavien-Dindo class III and IV) occurred in 5/22 patients in the STS group and 3/16 patients in the bone sarcoma group. The most common complication in both groups was deep wound infection requiring revision surgery under general anesthesia. One patient with STS developed respiratory insufficiency and required invasive ventilation. This patient later developed muscle flap necrosis and thrombosis of the contralateral free latissimus dorsi flap. The wound was finally covered with omentum and the infection was sanitized using vacuum-assisted closure. This patient was further treated on outpatient basis with chronic wound fistula. No class V complications were observed in either group.

Survival outcomes

Among patients with primary STS, during a median follow-up of 30 months (range, 9–110 months), 40% (4/10) developed local recurrence, distant metastasis, or both. Local recurrence was observed in one patient (5 months postoperatively), distant metastasis in one patient (16 months postoperatively), and both local recurrence and distant metastasis in two patients (6 and 12 months postoperatively). None of the patients with local recurrence received adjuvant treatment. All patients with disease relapse died within 2 years (9, 13, 15, and 19 months after surgery).

In the recurrent STS subgroup, during a median follow-up of 34 months (range, 6–77 months), 58.33% (7/12) of patients developed local recurrence or distant metastasis. Local recurrence was observed in two patients (12 and 35 months postoperatively), only one of whom received adjuvant radiotherapy, while distant metastasis occurred in five patients (2, 3, 18, 19, and 22 months postoperatively). Of the two patients with local recurrence, one died 54 months after the last operation, and the other underwent a second reoperation and is currently disease-free. Out of the five patients with distant metastasis, four died (at 6, 12, 27, and 39 months after the last operation) and one patient underwent resection of extrapulmonary metastasis and is currently disease-free.

Among patients with bone sarcoma, sufficient follow-up was performed in 15/16 patients. Among them, six patients experienced local recurrence or distant metastasis. Local recurrence was observed in 3/15 patients (8, 8, and 30 months postoperatively), all of whom had G2 chondrosarcoma, received no neoadjuvant or adjuvant therapy, and developed distant metastasis (8, 41, and 60 months postoperatively). Two of these patients died (18 and 57 months postoperatively), and one patient is still living with the disease. Distant metastasis without local recurrence was detected in two patients (6 and 15 months after resection), and in one patient, unexpected multiple lung metastases were identified intraoperatively, rendering the patient inoperable. All three patients with distant metastasis died (19, 25, and 26 months after surgery).

The Kaplan-Meier curves for OS, RFS, and MFS for the STS and bone sarcoma groups are shown in Figures 6,7, respectively. No statistically significant differences were observed between patients with primary and recurrent STS for any of the survival outcomes.

Figure 6 Survival analysis of STS patients. Kaplan-Meier curves depict the difference in (A) overall survival, (B) recurrence-free survival, and (C) metastasis-free survival. P values were calculated by log-rank test. STS, soft tissue sarcoma.

Figure 7 Survival analysis of patients with bone sarcoma. Kaplan-Meier curves depict the difference in (A) overall survival, (B) recurrence-free survival, and (C) metastasis-free survival. P values were calculated by log-rank test.

Factors influencing survival

In the Cox regression analysis, advanced disease and patient sex were significantly associated with OS. Namely, patients with metastases and local recurrence had a significantly higher mortality risk compared with those without advanced disease (P=0.002 and P=0.005, respectively). Additionally, female patients had a significantly higher mortality risk than male patients. In contrast, age and disease status (primary or recurrent) did not show associations with OS (Table 4).

Discussion

Key findings

This single-center case series provides insight into the outcomes of patients with primary and recurrent STS and bone sarcomas of the chest wall. In our cohort, the average tumor size ranged from 2.5 to 22.5 cm and the most prevalent STS and bone sarcoma subtypes were undifferentiated pleomorphic sarcoma and chondrosarcoma, respectively. All surgeries encompassed wide excisions, with R0 resection margins achieved in 95.45% and 93.75% of patients in the STS and bone sarcoma groups, respectively. Severe complications (Clavien-Dindo class III and IV) were observed in approximately 20% of all patients, with deep wound infection being the most common. No statistically significant differences were observed between patients with primary and recurrent STS for any of the survival outcomes. Advanced disease and female sex were significantly associated with OS.

Strengths and limitations

The main limitations of our study include the relatively small sample size, retrospective design, and significant heterogeneity among patients with different histological diseases despite the use of broad exclusion criteria. These factors impact the generalizability and interpretability of the results. Additionally, the retrospective design may introduce biases related to data collection and patient selection, further affecting the reliability of the findings. Future studies with larger, more homogeneous cohorts and prospective design would help to validate and extend our results. However, although randomized controlled studies on different histological types of sarcomas could potentially overcome these limitations, they are extremely difficult to devise given the rarity of STSs and especially rare STSs, which represent approximately 20% of all sarcomas (15).

Comparison with similar researches

Chest wall sarcomas often require extensive resections and complex reconstructions (7,8) that can lead to severe complications, considerably affecting patients’ quality of life. Several studies have highlighted the advantages of managing patients with sarcoma within high-volume, specialized reference centers, including improved OS (3-5,16). A recent study by van Roozendaal et al. provided a comprehensive overview of the management of chest wall STSs. Consistent with our findings, the study demonstrated that patients in whom R0 resection was achieved had significantly higher survival rates than those without clear surgical margins. The authors also underscored the necessity for individualized, multidisciplinary treatment approaches for these rare and heterogeneous tumors, further highlighting the importance of tailored therapeutic strategies and the involvement of a specialized, coordinated care team to optimize patient outcomes (17). We largely agree that treatment regimens should be determined by a multidisciplinary team to ensure comprehensive care.

The main objectives of surgery are achieving good oncological outcomes with little or no impact on patients’ quality of life. In study presented, all surgeries involved wide resections using the Enneking classification, with a liberal healthy margin, adapting the principles of aggressive surgery in retroperitoneal sarcomas (18-20). Surgeries performed by experienced thoracic surgeons had as high as 94.74% rate of R0 resection for STS and bone sarcoma in both primary and recurrent tumors combined, although differences were observed between patients with primary and recurrent tumors in terms of OS, RFS, and MFS. In our study, we observed extremely low adherence to clinical guidelines and treatment in a subgroup of patients with STS, resulting in 54.55% of patients requiring re-resection, consistent with the findings of Blay et al. (3). The high rate of disease recurrence could also be related to the fact that most patients had G2 or G3 tumors.

Explanations of findings

Most patients had either G2 or G3 tumors (Tables 1,2) resulting in higher rate or relapsed patients.

A pedicled latissimus dorsi flap is often used for reconstruction alone, with other flap types employed as needed. The latissimus dorsi flap is widely used in reconstructive plastic surgery, enabling immediate reconstruction with good clinical results and minimal morbidity associated with the loss of this muscle (21).

More severe complications (Clavien-Dindo class III and IV) and longer hospital stay were observed in patients who underwent re-resection. Consistent with prior findings, the most common severe complication in our cohort was deep wound infection requiring surgical revision under general anesthesia. Managing these infections is particularly challenging due to the presence of artificial materials, often resulting in multiple wound revisions, prolonged healing, and sometimes, removal of the osteosynthetic material. According to Dadras et al., prolonged antibiotic prophylaxis did not decrease the risk for infection, whereas it increased that for antibiotic-related adverse events (22). In the study of Bergovec et al., use of osteosynthetic materials for chest stabilization was associated with a higher risk for infections (23). In our study, all patients who were discharged within 30 days after surgery consistently reported no regular use of painkillers, no problems with breathing, and no impact on common daily activities.

Of the 38 patients included, only one patient with bone sarcoma had inadequate follow-up data. Clinical follow-up included contrast-enhanced CT and thoracic MRI every 6 months for G1 sarcomas, and every 3–4 months for G2 and G3 sarcomas over the first 3 years, which aligns with the findings of prior studies. MRI (and/or CT) can be used to evaluate local recurrence and is thus recommended to be performed at least once 3–4 months following resection of chest wall STSs and annually thereafter (17).

In terms of clinical outcomes, 17 out of 37 patients (45.95%) developed local recurrence, distant metastasis, or both. The large number of patients with disease recurrence is consistent with the findings of Collaud et al. (24). Although R0 resection was achieved in 35 out of 37 patients, local recurrence was observed in 8 (21.62%) patients, 7 of whom never received radiotherapy. Of the 12/14 patients who developed distant metastases, two are still alive. The most common site of relapse was the lungs. The survival analysis indicated that despite radical surgery, prognosis remains guarded, particularly for patients with high-grade tumors or metastatic disease. However, our analysis revealed that metastases, local recurrence, and female sex had a significant negative impact on OS, whereas no associations were observed for factors such as age and disease status (primary vs. recurrent). These findings underscore the importance of closely monitoring metastases and local recurrence in clinical practice and suggest a need for further investigation into sex-specific differences in OS.

In the present study, adjuvant radiotherapy was limited and selective, reflecting individualized approaches. Current clinical guidelines are not explicit regarding the use of neoadjuvant or adjuvant radiotherapy and chemotherapy in patients with localized disease (excluding Ewing disease and osteosarcoma) (6,25). The high rate of local recurrence justifies the use of radiotherapy, with many studies demonstrating its positive effect on local control, whether administered as neoadjuvant or adjuvant (26-28). Variables such as extent of resection, relationship to critical structures, and planned type of reconstruction must be considered for determining radiotherapy timing. Previous treatment is essential in chest wall sarcoma treatment, particularly for recurrent diseases and radiation-associated sarcomas. In our cohort, radiotherapy could not be indicated in many cases, mainly because of previous pretreatment and the impossibility of administering an adequate radiation dose. The most significant challenge remains decreasing the number of patients developing distant metastases. Currently, adjuvant chemotherapy is not a standard treatment after complete resection in patients with localized disease (6). However, some tumor subtypes exhibit greater sensitivity to conventional cytotoxic agents (29). Modern regimens including immunotherapy show limited data on STS (30), with various combinations of checkpoint inhibitor therapies evaluated but yielding unconvincing results (31).

Implications and actions needed

Our findings underscore the need for continued refinement in surgical techniques, adjuvant therapies, and follow-up strategies to improve the outcomes of patients with STS and bone sarcomas. The correlation between recurrence/metastasis and OS suggests that future research should focus on early detection and intervention strategies. Additionally, complications from extensive surgeries and reconstructions necessitate ongoing advancements in surgical techniques and postoperative care to mitigate these risks. Prospective multicenter studies with homogeneous cohorts are crucial but challenging to devise due to the rarity of the disease.

Conclusions

Chest wall sarcomas often require extensive resection and complex reconstruction. Although surgical treatment at reference sarcoma centers has significantly improved oncological and clinical outcomes, the prognosis of these patients remains guarded, necessitating further related research and continued refinement in surgical techniques, neo/adjuvant therapies, and follow-up strategies.

Acknowledgments

The authors thank all study participants and the dedicated clinical and technical staff for their assistance.

Funding: This work was supported by the Ministry of Health of the Czech Republic [grant No. AZV NU23J-08-00031] and the Cooperatio Program, Research Area SURG.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-472/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-472/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-472/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-472/coif). The 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 (as revised in 2013). The study was approved by the Ethics Committee for Multi-Centric Clinical Trials of the University Hospital Motol (Ref. EK-189/20) and 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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