Pulmonary metastasectomy in pediatric patients: a narrative review

Introduction

Approximately 25% of pediatric solid tumors present with metastatic disease at initial diagnosis, and another 20% will develop metastases during or after treatment (1). The majority of these metastases occur at pulmonary sites (1). While the mainstay of treatment for patients with solid tumors and pulmonary metastases is systemic therapy, surgical resection of metastases can offer therapeutic benefit. In 1961, Richardson first described pulmonary metastasectomy associated with pediatric solid tumors, which resulted in improved overall survival (OS) (2,3). Since then, multiple studies have addressed management principles for pulmonary metastasectomy (1-3). Among these included data to support the importance of tumor histology as well as the concept that factors such as the number of metastases and disease-free interval are not inherent contraindications to tumor resection (2). Many early reports from 1960 to 2000 grouped numerous tumor types together and precluded independent analysis of outcomes associated with pulmonary metastasectomy (2). In recent decades, differences in outcomes between oncologic histologies have been described, and the role of metastasectomy in pediatric solid malignancies has been evaluated. In general, tumors that are refractory to adjuvant therapies are most appropriate for pulmonary metastasectomy (1,3).

Depending on individual tumor subtype, estimates for OS in children with metastatic disease range from 20% to 70% (4). Regarding operative strategy, open thoracotomy is considered the traditional approach for resection of pulmonary nodules (5). However, it remains controversial whether more recent approaches such as video-assisted thoracoscopic surgery (VATS) are a suitable alternative to open thoracotomy for pulmonary metastasectomy (6). Special consideration is given to open resection as it permits palpation of lesions that may be missed on imaging (4,6). Recent technological improvements in radiological diagnostic imaging of pulmonary metastases and thoracoscopic resection have partially addressed the previously stated limitation in VATS for metastasectomy (5,7). In this narrative review, we summarize the existing data for outcomes of metastasectomy performed for common pediatric solid tumors associated with pulmonary metastases, the most common surgical approach, and post-operative outcomes. Those tumor types without multiple studies of outcomes after pulmonary metastasectomy in the pediatric population (neuroblastoma, adrenocortical carcinoma, etc.) were not discussed. We present this article in accordance with the Narrative Review reporting checklist (available at https://vats.amegroups.com/article/view/10.21037/vats-23-24/rc).

Methods

A comprehensive review of the literature published from January 1, 1990 to February 28, 2023 was completed by searches of the public databases the National Institute of Health National Library of Medicine PubMed and MEDLINE for published and indexed articles (Table 1). Studies and editorials written in languages other than English without an accompanying available translation were excluded.

Discussion

Solid tumors associated with pulmonary metastases treated by metastasectomy

Osteosarcoma

The management of pulmonary metastases is highly dependent on the associated primary tumor histology (2,3). For certain histologies, including osteosarcoma, surgical metastasectomy is often indicated and shown to be associated with improved patient survival (3). Osteosarcoma is the most common pediatric bone tumor capable of metastasizing to the lungs. Although OS has recently improved, metastatic disease has been a major determinant of prognosis with survival less than 34% in those presenting with metastases compared to 40–70% among all osteosarcoma patients (2,8,9). Pastorino et al. provided early evidence that aggressive surgical resection of all osteosarcoma metastases resulted in enhanced survival rates close to 68% and 58% at 3 and 5 years in their patient cohort, respectively (10,11). Others have described survival benefits after pulmonary metastasectomy for osteosarcoma only for those with peripheral lesions compared to central lesions (12). Factors that have been shown to be further associated with augmented survival include fewer numbers of metastases, histologic response to chemotherapeutic regimens, and prolonged disease-free periods (13-19). Several series have demonstrated that multiple thoracotomies may also allow some potential for cure with only mild reduction and effects on pulmonary function long-term (20-22). If both primary and metastatic sites can be completely resected, the majority of studies recommend pulmonary metastasectomy as part of a multidisciplinary approach to care for the pediatric population with osteosarcoma (4,9,15,23,24).

Ewing sarcoma

Ewing sarcoma is the second most common bone tumor in children with decreased survival for those with metastases (25). Given this malignancy’s sensitivity to chemotherapy and radiation, it remains controversial whether there is any effect on OS for patients treated with systemic therapy regardless of surgical resection (1,2,25). Some suggest a possible benefit for Ewing sarcoma patients who undergo pulmonary metastasectomy with one series demonstrating 5-year survival estimates in these patients approaching 80% compared to 0% among those not receiving surgical resection (25). A more recent study by Raciborska et al. of 38 patients with Ewing sarcoma of whom 23 received pulmonary metastasectomy following chemotherapy found improvements in event-free survival (EFS) with no clear benefit on OS (26). The authors concluded that resection of isolated metastases may play a role in therapy depending on histologic response to treatment. Overall, future studies are still needed to better delineate the advantages and selection criteria for individual patients with metastases secondary to Ewing sarcoma who are most likely to benefit from surgical intervention.

Hepatoblastoma

Pulmonary metastases present in approximately 20–44% of patients with hepatoblastoma and metastases are associated with a significantly lower survival rate compared to those without (1,27). Although some patients may demonstrate a complete response to systemic therapy, several series have ascribed benefits in EFS and OS for patients undergoing resection of metastatic hepatoblastoma sites. Early studies found benefits associated with metastatic resection in disease-free survival (DFS) in patients with recurrence if the recurrent sites occurred in isolation in the lung (28). Meyers et al. (29) recommended cautious utilization of thoracotomy for patients with both initial pulmonary metastases refractory to neoadjuvant chemotherapy as well as those with metastatic relapse. However, there was significant heterogeneity in timing and surgical approach within their patient population.

Pulmonary metastasectomy has been described as successful in achieving a disease-free state after resection of primary hepatoblastoma lesions. Shi et al. provided further evidence through a retrospective review of 10 patients with pulmonary metastatic recurrence to support the efficacy of surgical resection in hepatoblastoma patients with metastatic relapse (30). A recent retrospective comparative study by Fleming et al. (31) comprising 16 years and 50 patients with hepatoblastoma stratified patients by those who were high-risk versus not high-risk. They demonstrated that aggressive pursuit of no evidence of disease (NED) utilizing repeated pulmonary metastasectomy and complex local control strategies was associated with improved OS and EFS at 10 years (31). While future prospective studies and more standardized practices are needed, these series taken together support the utility of pulmonary metastasectomy for these patients.

Synovial sarcoma and other non-rhabdomyosarcoma soft tissue sarcomas (NRSTSs)

Synovial sarcoma is included in the family of NRSTS. Metastatic disease is present in up to 40% of patients with the majority (approximately 80%) occurring in the pulmonary system (1,32,33). Despite its responsiveness to systemic therapy compared to the rest of the NRSTS family, complete resection of metastatic disease is often recommended for synovial sarcoma (1). Slightly less than one-half of patients develop pulmonary metastases, emphasizing the importance of surgical resection (1). Stanelle et al. (34) compared a series of 41 patients with metastatic synovial sarcoma and found that those undergoing metastasectomy had an associated 5-year OS of 24%. Spillane et al. (33) similarly found an increase in OS of 17% among patients undergoing pulmonary metastasectomy compared to all patients. Taken together, these authors felt that metastasectomy was associated with survival benefits for children with synovial sarcoma if complete resection could be achieved.

Other NRSTS tumors such as chondroma sarcoma, malignant fibrous histiocytoma, and alveolar soft part sarcoma are also capable of metastasizing to pulmonary sites. Outcomes for these tumors are difficult to draw conclusions on given their rarity and resultantly few published series. Older series that examined a heterogeneous group of NRSTS including these types have ascribed greater disease control associated with pulmonary metastasectomy (35,36). However, survival outcomes were difficult to ascertain for different tumor subtypes. Kayton et al. (37) examined 20 patients with alveolar soft part sarcoma of which 14 were diagnosed with pulmonary metastases during their disease follow-up. OS at 5 years was 83% in this cohort, which led the authors to recommend metastasectomy for patients with pulmonary disease at presentation (37). Ultimately, more series with specific attention paid to outcomes after pulmonary metastasectomy are needed for patients with these rare tumor subtypes to draw more definitive recommendations on this procedure’s utility.

Operative strategy

Historically, open thoracotomy was undertaken for all cases of oncologic resection in children. Over the last few decades, minimally invasive surgery has become increasingly utilized for various procedures in adults and children and has disseminated to more frequent applications in pediatric oncology (38). The advantages are well known and include decreased post-operative pain, shorter hospital stay, and reduced tissue trauma (Figure 1) (38). Specifically, important benefits of thoracoscopy include reducing musculoskeletal complications associated with traditional thoracotomy such as chest wall deformities and scoliosis, which can occur in up to 30% of pediatric patients undergoing thoracotomy (38). Advantages associated with thoracotomy include the ability to evaluate the entire lung as well as the chance to directly palpate suspicious lesions and resect. This is particularly important for osseous tumors such as osteosarcoma that have a calcific matrix and can be felt in lesions as small as 1 mm, sometimes referred to as deposits (4). Osteosarcoma metastases in particular pose a diagnostic challenge given that they can frequently present with atypical radiological features or are unable to be adequately visualized even with high resolution computed tomography (CT) modalities as demonstrated in previous retrospective series (39-41).

Figure 1 Comparative operative approaches for pulmonary metastasectomy in children (the figure was created in Biorender.com).

VATS utilization increased rapidly from 2006 to 2009 and has plateaud in recent years (6). Challenges associated with VATS include reduced tactile feedback, smaller body size in pediatric patients, and limited working space (38). Despite the increased use of VATS for resection of lung metastases, controversy revolves around its inability to palpate lesions that can be missed on preoperative imaging such as those associated with osteosarcoma (6). Given the discordance between preoperative imaging detection of pulmonary metastases and intraoperative palpation of small deposits, this can be a contraindication for VATS in patients with osteosarcoma (41). For patients with other malignancies and concomitant solitary lung metastasis, Markowiak et al. demonstrated the equivalence of VATS for pulmonary metastasectomy to thoracotomy by providing evidence that an open approach with palpation of the lung showed no advantage in surgical outcome or survival (42). Traynor et al. (6) concluded VATS approaches for pulmonary metastasectomy resulted in fewer complications and shorter length of stay (LOS) in a nationwide sample of children even after controlling for resection extent, age and primary cancer.

As technology advances, combinations of approaches or adjunctive intraoperative imaging techniques may hold potential to augment the utility of VATS. Hybrid procedures combining VATS and lateral mini-thoracotomy to allow for manual palpation to perform multiple resections of pulmonary metastases has been described as a safe method to utilize the benefits of an open procedure while still accruing the reduced postoperative complication profile and LOS associated with VATS in adult series (43,44). In 1996, Gilbert et al. demonstrated VATS to be safe and complement open thoracotomy in children with osteosarcoma requiring pulmonary metastasectomy (45). With the increasing number of metastatic lesions, the use of stapler devices can be contraindicated with a higher number of resections and achieving a precision resection with VATS can be both time consuming and technically demanding (43,46). Laser-assisted resection may help to overcome some of these challenges and will require further study with regards to longer term OS and DFS prior to pediatric applications (47,48). Gow et al. (5) later illustrated that minimally invasive thoracoscopic ultrasound can be utilized to assist VATS to guide resection of deep pulmonary nodules intraoperatively for patients with osteosarcoma and other primary tumor types. Similarly, thoracoscopic resection of preoperatively localized small lung nodules via both CT-guided needle hook wire placement and microcoils has demonstrated as safe and effective in children (7,49,50). A recent survey of the American Pediatric Surgical Association reported that localization strategies are more frequently used by surgeons who prefer thoracoscopy for resection of pulmonary metastasis in children with osteosarcoma (51). Another emerging adjunct to guide visualization and resection strategies intraoperatively is using indocyanine green (ICG) fluorescence. To date, only case reports have demonstrated this application for pulmonary metastasectomy in the pediatric population (52,53). Furthermore, robotic-assisted thoracoscopic surgery (RATS) has rapidly gained utilization for oncologic resections in adults with beneficial results (54). No prospective pediatric series have yet to be performed with regards to RATS for pulmonary metastasectomy but may be an area of future investigation. Future studies are needed to determine if long term outcomes and relapse rates mirror the promising short-term results associated with newer approaches.

Conclusions

Metastatic disease for children continues to be associated with poor prognosis and survival compared to those with isolated primary tumors. Knowledge of the efficacy of pulmonary metastasectomy for pediatric solid tumors has significantly evolved over the past few decades. Although advancements in understanding the indications and outcomes associated with specific tumor histologies have been achieved, its role for primary tumors that are historically responsive to systemic therapy remains to be fully characterized. Additional research and data are necessary regarding the long-term outcomes associated with specific tumor histologies responsive to pulmonary metastasectomy.

Despite unique advantages and comparable post-operative outcomes of VATS with open thoracotomy, the use of VATS among pediatric surgeons has plateaued in recent years. This trend may be associated with limited prospective data regarding the long-term outcomes associated with open thoracotomy versus VATS for pulmonary metastasectomy in the pediatric population. The advent and role of hybrid VATS approaches including minithoracotomy may also help bridge the gap for oncologic applications such as these and be explored in future work. Areas of further study regarding its utilization should include whether indications for VATS in pulmonary metastasectomy can be expanded as well as potential intraoperative imaging adjuncts to guide resection as well as newer resection devices. Although significant strides in technological advancements for VATS continue to be made in adult patients, much remains to be studied to evaluate outcomes for pulmonary metastasectomy in this vulnerable patient population.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editors (Anthony W. Kim and Takashi Harano) for the series “The Role of Minimally Invasive Approaches in the Pulmonary Oligometastases” published in Video-Assisted Thoracic Surgery. The article has undergone external peer review.

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://vats.amegroups.com/article/view/10.21037/vats-23-24/rc

Peer Review File: Available at https://vats.amegroups.com/article/view/10.21037/vats-23-24/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://vats.amegroups.com/article/view/10.21037/vats-23-24/coif). The series “The Role of Minimally Invasive Approaches in the Pulmonary Oligometastases” was commissioned by the editorial office without any funding or sponsorship. The authors have no other 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.

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/.

References

1. Croteau NJ, Heaton TE. Pulmonary Metastasectomy in Pediatric Solid Tumors. Children (Basel) 2019;6:6. [Crossref] [PubMed]
2. Heaton TE, Davidoff AM. Surgical treatment of pulmonary metastases in pediatric solid tumors. Semin Pediatr Surg 2016;25:311-7. [Crossref] [PubMed]
3. Kayton ML. Pulmonary metastasectomy in pediatric patients. Thorac Surg Clin 2006;16:167-83. vi. [Crossref] [PubMed]
4. Scanagatta P, Girelli L. Metastasectomy in pediatric patients: indications, technical tips and outcomes. J Thorac Dis 2017;9:S1299-304. [Crossref] [PubMed]
5. Gow KW, Saad DF, Koontz C, et al. Minimally invasive thoracoscopic ultrasound for localization of pulmonary nodules in children. J Pediatr Surg 2008;43:2315-22. [Crossref] [PubMed]
6. Traynor MD, Brar GD, Bruno FP, et al. Pulmonary Metastasectomy in Pediatric Patients: A Comparison of Open and Thoracoscopic Approaches. J Laparoendosc Adv Surg Tech A 2021; Epub ahead of print. [Crossref] [PubMed]
7. Heran MK, Sangha BS, Mayo JR, et al. Lung nodules in children: video-assisted thoracoscopic surgical resection after computed tomography-guided localization using a microcoil. J Pediatr Surg 2011;46:1292-7. [Crossref] [PubMed]
8. Meazza C, Scanagatta P. Metastatic osteosarcoma: a challenging multidisciplinary treatment. Expert Rev Anticancer Ther 2016;16:543-56. [Crossref] [PubMed]
9. Kempf-Bielack B, Bielack SS, Jürgens H, et al. Osteosarcoma relapse after combined modality therapy: an analysis of unselected patients in the Cooperative Osteosarcoma Study Group (COSS). J Clin Oncol 2005;23:559-68. [Crossref] [PubMed]
10. Pastorino U, Gasparini M, Tavecchio L, et al. The contribution of salvage surgery to the management of childhood osteosarcoma. J Clin Oncol 1991;9:1357-62. [Crossref] [PubMed]
11. Pastorino U, Gasparini M, Valente M, et al. Primary childhood osteosarcoma: the role of salvage surgery. Ann Oncol 1992;3:S43-6. [Crossref] [PubMed]
12. Letourneau PA, Xiao L, Harting MT, et al. Location of pulmonary metastasis in pediatric osteosarcoma is predictive of outcome. J Pediatr Surg 2011;46:1333-7. [Crossref] [PubMed]
13. Gelderblom H, Jinks RC, Sydes M, et al. Survival after recurrent osteosarcoma: data from 3 European Osteosarcoma Intergroup (EOI) randomized controlled trials. Eur J Cancer 2011;47:895-902. [Crossref] [PubMed]
14. Buddingh EP, Anninga JK, Versteegh MI, et al. Prognostic factors in pulmonary metastasized high-grade osteosarcoma. Pediatr Blood Cancer 2010;54:216-21. [Crossref] [PubMed]
15. Harting MT, Blakely ML, Jaffe N, et al. Long-term survival after aggressive resection of pulmonary metastases among children and adolescents with osteosarcoma. J Pediatr Surg 2006;41:194-9. [Crossref] [PubMed]
16. Leary SE, Wozniak AW, Billups CA, et al. Survival of pediatric patients after relapsed osteosarcoma: the St. Jude Children's Research Hospital experience. Cancer 2013;119:2645-53. [Crossref] [PubMed]
17. Meyers PA, Heller G, Healey JH, et al. Osteogenic sarcoma with clinically detectable metastasis at initial presentation. J Clin Oncol 1993;11:449-53. [Crossref] [PubMed]
18. Briccoli A, Rocca M, Salone M, et al. High grade osteosarcoma of the extremities metastatic to the lung: long-term results in 323 patients treated combining surgery and chemotherapy, 1985-2005. Surg Oncol 2010;19:193-9. [Crossref] [PubMed]
19. Tsuchiya H, Kanazawa Y, Abdel-Wanis ME, et al. Effect of timing of pulmonary metastases identification on prognosis of patients with osteosarcoma: the Japanese Musculoskeletal Oncology Group study. J Clin Oncol 2002;20:3470-7. [Crossref] [PubMed]
20. Denbo JW, Zhu L, Srivastava D, et al. Long-term pulmonary function after metastasectomy for childhood osteosarcoma: a report from the St Jude lifetime cohort study. J Am Coll Surg 2014;219:265-71. [Crossref] [PubMed]
21. McCarville MB, Kaste SC, Cain AM, et al. Prognostic factors and imaging patterns of recurrent pulmonary nodules after thoracotomy in children with osteosarcoma. Cancer 2001;91:1170-6. [Crossref] [PubMed]
22. Temeck BK, Wexler LH, Steinberg SM, et al. Metastasectomy for sarcomatous pediatric histologies: results and prognostic factors. Ann Thorac Surg 1995;59:1385-9; discussion 1390. [Crossref] [PubMed]
23. Slade AD, Warneke CL, Hughes DP, et al. Effect of concurrent metastatic disease on survival in children and adolescents undergoing lung resection for metastatic osteosarcoma. J Pediatr Surg 2015;50:157-60; discussion 160. [Crossref] [PubMed]
24. Chou AJ, Kleinerman ES, Krailo MD, et al. Addition of muramyl tripeptide to chemotherapy for patients with newly diagnosed metastatic osteosarcoma: a report from the Children's Oncology Group. Cancer 2009;115:5339-48. [Crossref] [PubMed]
25. Letourneau PA, Shackett B, Xiao L, et al. Resection of pulmonary metastases in pediatric patients with Ewing sarcoma improves survival. J Pediatr Surg 2011;46:332-5. [Crossref] [PubMed]
26. Raciborska A, Bilska K, Rychłowska-Pruszyńska M, et al. Management and follow-up of Ewing sarcoma patients with isolated lung metastases. J Pediatr Surg 2016;51:1067-71. [Crossref] [PubMed]
27. Uchiyama M, Iwafuchi M, Naito M, et al. A study of therapy for pediatric hepatoblastoma: prevention and treatment of pulmonary metastasis. Eur J Pediatr Surg 1999;9:142-5. [Crossref] [PubMed]
28. Feusner JH, Krailo MD, Haas JE, et al. Treatment of pulmonary metastases of initial stage I hepatoblastoma in childhood. Report from the Childrens Cancer Group. Cancer 1993;71:859-64. [Crossref] [PubMed]
29. Meyers RL, Katzenstein HM, Krailo M, et al. Surgical resection of pulmonary metastatic lesions in children with hepatoblastoma. J Pediatr Surg 2007;42:2050-6. [Crossref] [PubMed]
30. Shi Y, Geller JI, Ma IT, et al. Relapsed hepatoblastoma confined to the lung is effectively treated with pulmonary metastasectomy. J Pediatr Surg 2016;51:525-9. [Crossref] [PubMed]
31. Fleming AM, Murphy AJ, Sarvode Mothi S, et al. Aggressive Pursuit of No Evidence of Disease Status in Hepatoblastoma Improves Survival: An Observational Study. J Pediatr Surg 2023;58:1081-7. [Crossref] [PubMed]
32. Andrassy RJ, Okcu MF, Despa S, et al. Synovial sarcoma in children: surgical lessons from a single institution and review of the literature. J Am Coll Surg 2001;192:305-13. [Crossref] [PubMed]
33. Spillane AJ, A'Hern R, Judson IR, et al. Synovial sarcoma: a clinicopathologic, staging, and prognostic assessment. J Clin Oncol 2000;18:3794-803. [Crossref] [PubMed]
34. Stanelle EJ, Christison-Lagay ER, Wolden SL, et al. Pulmonary metastasectomy in pediatric/adolescent patients with synovial sarcoma: an institutional review. J Pediatr Surg 2013;48:757-63. [Crossref] [PubMed]
35. Pappo AS, Rao BN, Jenkins JJ, et al. Metastatic nonrhabdomyosarcomatous soft-tissue sarcomas in children and adolescents: the St. Jude Children's Research Hospital experience. Med Pediatr Oncol 1999;33:76-82. [Crossref] [PubMed]
36. Dillon P, Maurer H, Jenkins J, et al. A prospective study of nonrhabdomyosarcoma soft tissue sarcomas in the pediatric age group. J Pediatr Surg 1992;27:241-4; discussion 244-5. [Crossref] [PubMed]
37. Kayton ML, Meyers P, Wexler LH, et al. Clinical presentation, treatment, and outcome of alveolar soft part sarcoma in children, adolescents, and young adults. J Pediatr Surg 2006;41:187-93. [Crossref] [PubMed]
38. Riccipetitoni G, Bertozzi M, Gazzaneo M, et al. The Role of Video-Assisted Thoracoscopic Surgery in Pediatric Oncology: Single-Center Experience and Review of the Literature. Front Pediatr 2021;9:721914. [Crossref] [PubMed]
39. Silva JAM, Marchiori E, Amorim VB, et al. CT features of osteosarcoma lung metastasis: a retrospective study of 127 patients. J Bras Pneumol 2023;49:e20220433. [PubMed]
40. Cai Z, Xu J, Sun X, et al. How to confront the high prevalence of pulmonary micro nodules (PMNs) in osteosarcoma patients? Int Orthop 2022;46:2425-36. [Crossref] [PubMed]
41. Gao E, Li Y, Zhao W, et al. Necessity of thoracotomy in pulmonary metastasis of osteosarcoma. J Thorac Dis 2019;11:3578-83. [Crossref] [PubMed]
42. Markowiak T, Dakkak B, Loch E, et al. Video-assisted pulmonary metastectomy is equivalent to thoracotomy regarding resection status and survival. J Cardiothorac Surg 2021;16:84. [Crossref] [PubMed]
43. Sauvain MO, Abdelnour-Berchtold E, Zellweger M, et al. Why choosing a video-assisted thoracic surgery approach for pulmonary metastasectomy? J Vis Surg 2019;5:46. [Crossref]
44. Raza A, Takabe K, Wolfe LG, et al. Outcomes of Hybrid Video Assisted Thoracoscopic Surgery for Pulmonary Metastasectomy. J Surg Sci 2014;2:18-24. [PubMed]
45. Gilbert JC, Powell DM, Hartman GE, et al. Video-assisted thoracic surgery (VATS) for children with pulmonary metastases from osteosarcoma. Ann Surg Oncol 1996;3:539-42. [Crossref] [PubMed]
46. Welter S, Gupta V. Algorithm for the pulmonary metastasectomy based on number of metastases and histology. Video-assist Thorac Surg 2021;6:35. [Crossref]
47. Mc Loughlin JB, O'Sullivan KE, Brown RH, et al. Limax Nd:YAG laser-assisted thoracoscopic resection of pulmonary metastases; a single centre's initial experience. Ir J Med Sci 2019;188:771-6. [Crossref] [PubMed]
48. Meyer C, Bartsch D, Mirow N, et al. Video-Assisted Laser Resection of Lung Metastases-Feasibility of a New Surgical Technique. Thorac Cardiovasc Surg 2017;65:382-6. [Crossref] [PubMed]
49. Parida L, Fernandez-Pineda I, Uffman J, et al. Thoracoscopic resection of computed tomography-localized lung nodules in children. J Pediatr Surg 2013;48:750-6. [Crossref] [PubMed]
50. Morgan KM, Crowley JJ, Many BT, et al. Microcoil localization as an effective adjunct to thoracoscopic resection of pulmonary nodules in children. J Pediatr Surg 2021;56:142-5. [Crossref] [PubMed]
51. Lautz TB, Krailo MD, Han R, et al. Current surgical management of children with osteosarcoma and pulmonary metastatic disease: A survey of the American Pediatric Surgical Association. J Pediatr Surg 2021;56:282-5. [Crossref] [PubMed]
52. Delgado-Miguel C, Estefanía K, San Basilio M, et al. Indocyanine green navigation in minimally invasive resection of multiple metachronous pulmonary metastases of hepatoblastoma. Thorac Cancer 2023;14:528-32. [Crossref] [PubMed]
53. Komatsu S, Terui K, Nakata M, et al. Combined Use of Three-Dimensional Construction and Indocyanine Green-Fluorescent Imaging for Resection of Multiple Lung Metastases in Hepatoblastoma. Children (Basel) 2022;9:376. [Crossref] [PubMed]
54. Yang MZ, Tan ZH, Li JB, et al. Comparison of Short-Term Outcomes Between Robot-Assisted and Video-Assisted Segmentectomy for Small Pulmonary Nodules: A Propensity Score-Matching Study. Ann Surg Oncol 2023;30:2757-64. [Crossref] [PubMed]