Optimizing outcomes in symptomatic spinal metastases from non-small cell lung cancer: Evaluating the role of salvage surgical intervention in a multidisciplinary context – A Narrative Review

Review

Hell J Surg. 2024 Jan-Mar;94(1):13–19
doi: 10.59869/23023

Eleftherios Nikolaidis1, Vasileios Leivaditis2, Nikolaos Bolanos1,  Dimitrios Anagnostopoulos1, Konstantinos Grapatsas3, Efstratios Koletsis4, Athanasios Papatriantafyllou2, Francesk Mulita5, Levan Tchabashvili5, Konstantinos Tasios5, Nikolaos Baltayiannis1, Manfred Dahm2, Antonios Chatzimichalis1

1Department of Thoracic Surgery, ‘’Metaxa’’ Cancer Hospital,Piraeus,Greece
2Department of Cardiothoracic and Vascular surgery, Westpfal-Klinikum, Kaiserslautern, Germany
3Department of Thoracic Surgery and Thoracic Endoscopy, University Medicine Essen – Ruhrlandklinik, Essen, Germany
4Department of Cardiothoracic Surgery, University Hospital of Patras, Patras, Greece, 5Department of General Surgery, University Hospital of Patras, Patras, Greece


Correspondence:  Francesk Mulita MD, MSc, PhD Resident Surgeon at the Department of Surgery, General University Hospital of Patras, Achaia, Greece, Tel.: +30 6982785142, e-mail: oknarfmulita@hotmail.com, ORCID Id: https://orcid.org/0000-0001-7198-2628


Abstract

Background: Lung cancer, a leading cause of cancer-related mortality worldwide, often metastasises to the spine, resulting in significant morbidity and complex treatment challenges. The management of spinal metastatic disease from lung cancer necessitates a multidisciplinary approach, given the array of potential interventions including surgery, radiation therapy, chemotherapy, and supportive care. The selection of appropriate therapeutic strategies is influenced by multiple factors, including disease staging, patient health status, and symptomatology.

Aim: This review article aims to explore the current landscape of surgical intervention for spinal metastases from lung cancer, evaluating its role, efficacy, and the criteria for patient selection within the context of multidisciplinary care. Additionally, it seeks to provide an overview of the existing treatment modalities, highlighting the importance of a tailored approach based on individual patient needs.

Methods: An extensive review of the literature was conducted, focusing on studies, clinical trials, and meta-analyses published on the treatment of spinal metastases in lung cancer patients. Special attention was given to works discussing the surgical outcomes, prognostic factors, and the evolution of treatment protocols over recent decades.

Results: Surgical treatment for spinal metastases from lung cancer is beneficial for select patients, particularly those without prior systemic treatments and those in good overall health. The decision to pursue surgery should be made within a multidisciplinary team, taking into account the patient’s specific situation and potential to benefit from the intervention. Research advancements and technological innovations continue to refine surgical techniques and improve patient outcomes.

Conclusion: While the role of surgery in treating spinal metastatic disease from lung cancer is limited, it remains a critical option for appropriately selected patients. Future research should aim to further define and expand the criteria for surgical candidacy, enhancing the precision of patient selection and tailoring of treatment strategies. Emphasis on a multidisciplinary approach is essential for optimising outcomes and advancing care for patients with this challenging condition.

Key Words: Non-small cell lung cancer, small cell lung cancer, spinal metastases, bone metastasis, spinal cord compression, osteolytic metastasis, surgical intervention, multidisciplinary approach


Submission: 02.12.2023, Acceptance: 02.04.2024


INTRODUCTION

Lung cancer stands as a predominant cause of mortality attributed to cancer worldwide, with classification into two primary types: small cell lung cancer (SCLC) and non-small cell lung cancer (NSCLC). A prevalent complication observed in the advanced stages of lung cancer is spinal metastasis, which involves the dissemination of cancer cells from the primary tumour site to the vertebral column. This condition results in significant clinical manifestations, including pain, neurological impairment, and a spectrum of other debilitating symptoms. Lung cancer is identified as the principal origin for approximately 80% of spinal metastases, positioning the skeletal system as the third most common site for cancer metastases, following the liver and lungs. Metastases of the osteolytic type, notably from the lung, kidney, thyroid, and gastrointestinal tract, are particularly concerning [1,2].

Extensive review of relevant literature and clinical observations have established that spinal metastases constitute the most frequent complication among cancer patients, affecting roughly 70% of individuals diagnosed with cancer. Given that lung cancer is the foremost cancer type to metastasise to skeletal structures, it is anticipated that a minimum of 40% of individuals with lung cancer will develop bone metastases throughout their disease trajectory [3]. The emergence of bone metastasis significantly impacts patients’ independence, functionality, and quality of life, while also escalating disability, mortality rates, hospitalization costs, and duration of hospital stays [4,5]. Metastatic involvement of the vertebral column is recognised as a distressing condition that adversely affects morbidity, functional disability, and survival expectancy. Reports indicate that nearly half of the individuals succumbing to cancer have vertebral column metastases, with 10% experiencing spinal cord compression [6].

This manuscript aims to explore the clinical scenario of lung cancer metastasizing to the spine and the role of surgical intervention as a palliative measure in select cases. It is critical to underline that the option of surgical treatment remains a subject of debate, and the surgical approach is sometimes viewed with skepticism. This stems from the fact that surgical intervention is not traditionally included within the conservative management spectrum for lung cancer but is considered for cases exhibiting progressive neurological deficits [7].

METHODOLOGY

In conducting this review, a comprehensive literature search was performed across several major databases, including PubMed, Scopus, and Web of Science, to gather relevant information on the surgical management of spinal metastases from non-small cell lung cancer. The search strategy employed a combination of keywords such as “non-small cell lung cancer,” “spinal metastasis,” “surgical treatment,” “multidisciplinary approach,” and “patient outcomes.” The selection criteria were focused on articles published in English, with a particular emphasis on clinical trials, observational studies, and meta-analyses that discussed outcomes, prognostic factors, and the evolution of surgical and multidisciplinary treatments for spinal metastases in lung cancer patients. This methodological approach enabled the identification and synthesis of critical insights into the current state and future directions of surgical care for spinal metastases from non-small cell lung cancer.

EPIDEMIOLOGY, PATHOPHYSIOLOGY AND DIAGNOSIS

Spinal metastasis represents a common complication in lung cancer, affecting approximately 20-40% of patients in the advanced stages of the disease. The likelihood of developing spinal metastases escalates as lung cancer progresses, with a higher prevalence observed in individuals diagnosed with NSCLC compared to those with SCLC [3-5]. Approximately 60-70% of SCLC patients will have extensive disease at diagnosis, with a significant portion developing spinal metastases. SCLC’s rapid growth and early dissemination patterns contribute to this higher rate of spinal involvement. However, while NSCLC has a lower overall metastatic rate at diagnosis compared to SCLC, the higher prevalence of NSCLC means it also contributes significantly to the number of spinal metastases cases [1-4]. The underlying mechanisms of spinal metastasis in lung cancer are intricate and involve multiple factors. Cancer cells can colonise the spine via hematogenous spread, lymphatic dissemination, or direct invasion of adjacent tissues. This metastatic involvement can lead to spinal cord or nerve root compression, manifesting as pain, neurological deficits, and a range of other clinical symptoms. Furthermore, pathological fractures of the spine due to metastatic lesions significantly contribute to patient morbidity [4,5].

Diagnosing spinal metastases in lung cancer poses considerable challenges and necessitates an integrated approach that includes detailed patient history, physical examination, and diagnostic imaging. Tools such as X-rays, computed tomography (CT) scans, and magnetic resonance imaging (MRI) are pivotal in the assessment and identification of spinal metastases. In certain scenarios, biopsy or the acquisition of tissue samples may be imperative to establish a definitive diagnosis [4-6].

SURGICAL MANAGEMENT OF LUNG CANCER WITH SPINAL INVASION

Lung cancer frequently exhibits growth and intrathoracic spread, alongside metastases to various organs. Predominant metastatic sites include supraclavicular and inferior cervical lymph nodes, liver, brain, bones, and adrenal glands [4,5]. Approximately 40% of patients with lung cancer develop bone metastases, predominantly of the osteolytic type, leading to significant morbidity. This includes pathological fractures, nerve root compression, bone pain, spinal cord compression, neoplastic bone marrow infiltration, and hypercalcemia of malignancy. These complications arise from increased bone metabolism, primarily due to enhanced bone resorption, and are managed through radiation therapy, specific radioisotope administration, surgical intervention, and analgesic treatment [3].

The onset of lung cancer metastases to the vertebral column can occur at any stage of the disease, through direct extension, hematogenous spread, or lymphatic routes. While these tumours are generally considered incurable, advancements in technology have enabled the possibility of radical surgical interventions [2]. Remarkably, 10% of patients with vertebral metastases are unaware of their cancer diagnosis, with spinal cord compression often being the initial presenting symptom; 5% of these cases are due to lung cancer [7]. Lung tumours typically develop osteolytic metastases, demonstrating a tendency for osteotropy. The radiographic appearance of bone metastases varies based on the degree of osteolysis or bone formation, the primary tumour, and its location [9].

The impact of malignancies on the vertebral column includes structural weakness, ataxia, and severe pain, necessitating immediate surgical intervention for stabilization [10]. Primary lung tumours invading the spine can cause excruciating pain and Horner syndrome, with the pain intensifying as the cancer progressively destroys vertebral bodies [2,11].

Following the findings from a randomised trial by Patchell et al. in 2005, the importance of decompressive surgical resection in managing metastatic spinal cord compression has been established [12]. The goal of surgical treatment is to decompress the spinal canal by removing the tumour mass. This is complemented by minimally invasive techniques such as spondylodesis for vertebral column stabilization and spondylosyndesis through various surgical approaches, alongside kyphoplasty and stereotactic radiotherapy. Surgical management of vertebral metastasis is primarily palliative, focusing on spinal canal decompression and stability restoration [13].

Percutaneous vertebral augmentation techniques, like percutaneous kyphoplasty (PKP) and percutaneous vertebroplasty (PVP), offer minimally invasive alternatives for managing painful spinal metastases, especially in high-risk patients [14,15]. Studies by Zhang et al. have shown PKP to significantly correct kyphosis compared to conservative treatments, providing substantial pain relief and functional improvement while preventing further local kyphotic deformation [15]. Direct decompressive surgery followed by postoperative radiotherapy has proven more effective than radiotherapy alone in improving muscle strength, functional capability, and overall survival rates [16].

However, the utility of PKP in a palliative setting does not extend to improving patient survival rates, despite enhancing quality-adjusted life years (QALY) and indicating improved life quality post-treatment [17]. The surgical approach for lung tumours invading the spine and its contribution to cancer therapy remains a topic of debate, with clinical evidence indicating poor survival rates post-surgical treatment for spinal involvement due to lung cancer [10,17].

It is crucial to evaluate prognostic factors in the decision-making process for treating bone metastases in lung cancer. Tokuhashi et al. proposed six prognostic factors for assessing survival chances in patients with metastatic vertebral column tumours, including (i) the number of vertebral metastases, (ii) the presence of internal organ translocations, (iii) the severity of spinal cord paralysis, (iv) the patient’s overall health condition, and (v) the presence of non-vertebral bone metastases [18].

The revised Tokuhashi, Tomita, modified Bauer, and Oswestry scores are frequently utilised as tools for predicting the survival of patients with spinal metastases and assisting in the decision-making process concerning surgical interventions [19-22]. Nevertheless, these prognostic indicators often provide a prognosis for patients with lung cancer that is more pessimistic than warranted. Studies showed that the Tokuhashi scores outperformed the Tomita score; nonetheless, they continued to provide prognostic estimates that were too low for 35% to 40% of the patients [23].

Other prognostic factors, including the number of bone metastases, the primary tumour’s malignancy degree, and visceral metastasis to major organs, play a critical role in assessing the feasibility and utility of surgical interventions in the vertebral column [20]. Prognosis remains particularly poor for patients with bone metastases, metastases to vital organs, and direct spinal invasion, especially in cases of superior sulcus tumours [24-27]. Therefore, the decision to proceed with surgical intervention in patients with lung cancer invading the spine requires a multidisciplinary approach. Considerations for total vertebrectomy should be discussed when direct invasion involves 30% or less of the vertebral cortical bone, with preoperative and postoperative chemoradiotherapy deemed sufficient for disease recurrence prevention [28].

In conclusion, the surgical management of lung cancer with spinal invasion is complex and controversial, potentially beneficial for severe pain management and tumour recurrence control [29,30]. Complete resection and multilevel laminectomy may be proposed for extensive tumour invasion, while partial vertebrectomy is suggested for less extensive tumour involvement. This underscores the need for aggressive, multidisciplinary surgical strategies, particularly for superior sulcus tumours with vertebral invasion, to improve prognosis and survival rates [31-33].

DISCUSSION

Presently, lung cancer is acknowledged as one of the deadliest cancers, with spinal metastases deemed generally incurable. Metastatic spread to the thoracic spine from lung cancer, which can occur via lymphatic or hematogenous routes, is notably frequent [34]. The consideration of surgical intervention for metastatic lung cancer infiltrating the spine presents a formidable challenge, marked by debate. The characteristics of the metastasis, including the organs involved, extent of infiltration, number of bone metastases, severity of spinal cord impairment, and level of pain, are critical prognostic factors that influence both the surgical outcomes and the patient’s survival prospects [34,35].

The prognosis plays a pivotal role in deciding the appropriateness of surgical intervention. Consequently, there’s a notable hesitancy to opt for surgery in patients with a limited life expectancy, compounded by a scarcity of studies and data supporting surgical intervention in such patient demographics [35]. The prognostic scoring systems developed in the 1990s and early 2000s, such as the Tokuhashi score, are commonly utilised to assess patients with a grim prognosis. However, the reliability and predictive accuracy of these tools have been questioned, as they often fail to accurately forecast survival, leading to potential underutilization in surgical candidate selection [35,36]. Lee et al. highlighted that the actual survival of patients frequently surpassed the expectations set by the revised Tokuhashi score, suggesting an improvement in survival rates due to advancements in medical and surgical oncology, which complicates the prognosis prediction [37]. Therefore, it is crucial to reevaluate the exclusion criteria to ensure that patients who could benefit from surgery are not inadvertently overlooked.

In the surgical treatment planning process, spine surgeons should be mindful of the tendency to underestimate patient survival. Notably, patients who have not previously received systemic treatment might benefit more substantially from surgery. Factors such as low BMI, indicative of a cachectic state, may predict a worse prognosis and should be considered in the evaluation process. Ideal surgical candidates include those with adenocarcinoma amenable to targeted therapies, candidates for denosumab treatment, individuals in good general health, and those yet to undergo systemic treatments [23].

Historically, surgical treatment for lung cancer with spinal invasion has yielded disappointing long-term outcomes concerning both mortality and morbidity, particularly in advanced-stage patients. Such conditions have been characterised as incurable and unresectable, with a poor long-term prognosis, especially in cases of vertebral invasion by superior sulcus tumours [38]. However, Yokomise et al. reported that advancements in technology and the introduction of novel surgical techniques have the potential to enhance surgical outcomes [32]. Recent studies have demonstrated the efficacy of multimodal treatment, including surgical resection for selected patients with superior sulcus tumours involving the spine, showcasing safe procedures with promising survival rates following concurrent chemoradiotherapy (CRT) and surgical resection, resulting in a 5-year overall survival (OS) and disease-free survival (DFS) rate of 55% and 40%, respectively [39].

Park et al. aimed to analyse survival and functional outcomes post-surgery in patients with spinal metastases and limited life expectancy, reviewing 492 surgical cases across different time frames. The study found a significant improvement in median survival, particularly in the latest period studied (2013–2020), with notable survival enhancements for lung and kidney cancer cases within this timeframe [40]. Moreover, hybrid therapy involving separation surgery followed by stereotactic body radiation therapy in NSCLC patients with metastatic epidural spinal cord compression has shown high local control rates and survival benefits when combined with Epidermal Growth Factor Receptor (EGFR) -targeted treatments initiated post-hybrid therapy [41].

A recent meta-analysis systematically reviewed prognostic factors and outcomes of surgical intervention for lung cancer patients with spinal metastases, covering 14 studies and 813 patients. The analysis identified preoperative ambulatory status and the number of involved vertebrae as significant prognostic factors influencing survival. The study suggests that patients with an adequate expected survival period could gain from surgical intervention, particularly when combined with adjuvant therapies [42].

Consequently, a deeper understanding of metastatic disease pathophysiology and technological advancements has the potential to refine surgical techniques, improving prognosis and extending survival for appropriately selected patient groups. Despite the constrained role of surgery in the overarching management of spinal metastatic disease from lung cancer, its potential benefits for specific patient cohorts should not be overlooked. Future perspectives should focus on refining patient selection criteria and enhancing surgical techniques through research and technological advancements. These efforts promise to better delineate the role of surgery within a multifaceted treatment approach, aiming for improved survival rates and quality of life for patients facing this challenging diagnosis.

CONCLUSION

The surgical approach, while not the universal standard, plays a pivotal role in the management of spinal metastatic disease from lung cancer for select patients. This necessitates precise diagnosis and tailored interventions, considering the disease’s stage, patient’s health, and symptom severity. Treatment strategies, often encompassing surgery, radiation, chemotherapy, and supportive care, aim to alleviate symptoms and enhance life quality. Identifying candidates for surgery requires a multidisciplinary approach, emphasizing the need for collaborative planning and evaluation by a team of specialists to ensure the most beneficial outcomes. Ongoing research is crucial to unravel the complexities of spinal metastasis and to innovate more effective treatments. Understanding the mechanisms of metastasis and improving therapeutic options will ultimately enhance patient management and prognosis. Thus, while surgery offers significant benefits for certain patients, its application should be carefully considered within a comprehensive, patient-focused, and multidisciplinary treatment framework.

Ethical standards declaration: Ethical approval was not obtained from the medical research ethics committee, due to the nature of this study.

Conflict of interest: There are no conflicts of interest to declare.

REFERENCES
  1. Papagelopoulos PJ, Savvidou OD, Galanis EC, Mavrogenis AF, Jacofsky DJ, Frassica FJ, et al. Advances and challenges in diagnosis and management of skeletal metastases. Orthopedics. 2006 Jul;29(7):609-20; Quiz 621-2.
  2. Ratliff JK, Cooper PR. Metastatic spine tumors. South Med J. 2004 Mar;97(3):246-53.
  3. Coleman RE. Metastatic bone disease: clinical features, pathophysiology and treatment strategies. Cancer Treat Rev. 2001 Jun;27(3):165-76.
  4. Berenson JR, Rajdev L, Broder M. Managing bone complications of solid tumors. Cancer Biol Ther. 2006 Sep;5(9):1086-9.
  5. Botteman M, Foley I, Marfatia A, Brandman J, Langer C. Economic value of Zoledronic acid versus placebo in the treatment of skeletal metastases in patients with lung cancer: The case of the United Kingdom (UK). J Clin Oncol. 2007 Jun;25(18_suppl):6617.
  6. Sundaresan N, Digiacinto GV, Hughes JE, Cafferty M, Vallejo A. Treatment of neoplastic spinal cord compression: results of a prospective study. Neurosurgery. 1991 Nov;29(5):645-50.
  7. Aydinli U, Ozturk C, Bayram S, Sarihan S, Evrensel T, Yilmaz HS. Evaluation of lung cancer metastases to the spine. Acta Orthop Belg. 2006 Oct;72(5):592-7.
  8. Maisano R, Pergolizzi S, Cascinu S. Novel therapeutic approaches to cancer patients with bone metastasis. Crit Rev Oncol Hematol. 2001 Dec;40(3):239-50.
  9. Peh WC, Muttarak M. Clinics in diagnostic imaging (82). Lesser trochanter metastasis. Singapore Med J. 2003 Feb;44(2):101-5.
  10. Chen YJ, Chang GC, Chen HT, Yang TY, Kuo BI, Hsu HC, et al. Surgical results of metastatic spinal cord compression secondary to non-small cell lung cancer. Spine (Phila Pa 1976). 2007 Jul;32(15):E413-8.
  11. Komagata M, Nishiyama M, Imakiire A, Kato H. Total spondylectomy for en bloc resection of lung cancer invading the chest wall and thoracic spine. Case report. J Neurosurg. 2004 Apr;100(4 Suppl Spine):353-7.
  12. Patchell RA, Tibbs PA, Regine WF, Payne R, Saris S, Kryscio RJ, et al. Direct decompressive surgical resection in the treatment of spinal cord compression caused by metastatic cancer: A randomised trial. Lancet. 2005 Aug;366(9486):643-8.
  13. Jacobs WB, Perrin RG. Evaluation and treatment of spinal metastases: An overview. Neurosurg Focus. 2001 Dec;11(6):e10.
  14. Zhang JX, Song ZR, Zou J, Ge J, Yang HL. Balloon kyphoplasty as palliative care for painful pathological spinal fracture followed by lung cancer metastasis: A cohort study. Front Surg [Internet]. 2023 Jan;9:1081823. Available from: https://pubmed.ncbi.nlm.nih.gov/36733676/
  15. Wang Y, Liu H, Pi B, Yang H, Qian Z, Zhu X. Clinical evaluation of percutaneous kyphoplasty in the treatment of osteolytic and osteoblastic metastatic vertebral lesions. Int J Surg. 2016 Jun;30:161-5.
  16. Bartels RH, van der Linden YM, van der Graaf WT. Spinal extradural metastasis: review of current treatment options. CA Cancer J Clin. 2008 Jul-Aug;58(4):245-59.
  17. Weigel B, Maghsudi M, Neumann C, Kretschmer R, Müller FJ, Nerlich M. Surgical management of symptomatic spinal metastases. Postoperative outcome and quality of life. Spine (Phila Pa 1976). 1999 Nov;24(21):2240-6.
  18. Tokuhashi Y, Matsuzaki H, Toriyama S, Kawano H, Ohsaka S. Scoring system for the preoperative evaluation of metastatic spine tumor prognosis. Spine (Phila Pa 1976). 1990 Nov;15(11):1110-3.
  19. Tokuhashi Y, Matsuzaki H, Oda H, Oshima M, Ryu J. A revised scoring system for preoperative evaluation of metastatic spine tumor prognosis. Spine (Phila Pa 1976). 2005 Oct;30(19):2186-91.
  20. Tomita K, Kawahara N, Kobayashi T, Yoshida A, Murakami H, Akamaru T. Surgical strategy for spinal metastases. Spine (Phila Pa 1976). 2001 Feb;26(3):298-306.
  21. Leithner A, Radl R, Gruber G, Hochegger M, Leithner K, Welkerling H, et al. Predictive value of seven preoperative prognostic scoring systems for spinal metastases. Eur Spine J. 2008 Nov;17(11):1488-95.
  22. Balain B, Jaiswal A, Trivedi JM, Eisenstein SM, Kuiper JH, Jaffray DC. The Oswestry Risk Index: an aid in the treatment of metastatic disease of the spine. Bone Joint J. 2013 Feb;95-B(2):210-6.
  23. Huang AP, Yang CY, Xiao F, Yang SH, Chen CM, Lai DM, et al. Spinal metastases from non-small cell lung cancer – Is surgical extent enough by following suggestions of the Tomita and Tokuhashi scores? Asian J Surg. 2023 Sep:S1015-9584(23)01332-5.
  24. Hansen BH, Keller J, Laitinen M, Berg P, Skjeldal S, Trovik C, et al. The scandinavian sarcoma group skeletal metastasis register. Survival after surgery for bone metastases in the pelvis and extremities. Acta Orthop Scand Suppl. 2004 Apr;75(311):11-5.
  25. Katagiri H, Takahashi M, Wakai K, Sugiura H, Kataoka T, Nakanishi K. Prognostic factors and a scoring system for patients with skeletal metastasis. J Bone Joint Surg Br. 2005 May;87(5):698-703.
  26. van der Linden YM, Dijkstra SP, Vonk EJ, Marijnen CA, Leer JW. Dutch Bone Metastasis Study Group. Prediction of survival in patients with metastases in the spinal column: results based on a randomized trial of radiotherapy. Cancer. 2005 Jan;103(2):320-8.
  27. Sartori F, Rea F, Calabrò F, Mazzucco C, Bortolotti L, Tomio L. Carcinoma of the superior pulmonary sulcus. Results of irradiation and radical resection. J Thorac Cardiovasc Surg. 1992 Sep;104(3):679-83.
  28. Rusch VW, Giroux DJ, Kraut MJ, Crowley J, Hazuka M, Johnson D, et al. Induction chemoradiation and surgical resection for non-small cell lung carcinomas of the superior sulcus: Initial results of Southwest Oncology Group Trial 9416 (Intergroup Trial 0160). J Thorac Cardiovasc Surg. 2001 Mar;121(3):472-83.
  29. Ginsberg RJ, Martini N, Zaman M, Armstrong JG, Bains MS, Burt ME, et al. Influence of surgical resection and brachytherapy in the management of superior sulcus tumor. Ann Thorac Surg. 1994 Jun;57(6):1440-5.
  30. Komaki R, Mountain CF, Holbert JM, Garden AS, Shallenberger R, Cox JD, et al. Superior sulcus tumors: Treatment selection and results for 85 patients without metastasis (Mo) at presentation. Int J Radiat Oncol Biol Phys. 1990 Jul;19(1):31-6.
  31. Grunenwald DH, Mazel C, Girard P, Veronesi G, Spaggiari L, Gossot D, et al. Radical en bloc resection for lung cancer invading the spine. J Thorac Cardiovasc Surg. 2002 Feb;123(2):271-9.
  32. Yokomise H, Gotoh M, Okamoto T, Yamamoto Y, Ishikawa S, Liu D, et al. En bloc partial vertebrectomy for lung cancer invading the spine after induction chemoradiotherapy. Eur J Cardiothorac Surg. 2007 May;31(5):788-90.
  33. Spaggiari L, Rusca M, Carbognani P, Solli P. Hemivertebrectomy for apical chest tumors: is the risk justified by the outcome? Ann Thorac Surg. 1998 May;65(5):1515-7.
  34. Kaloostian PE, Zadnik PL, Etame AB, Vrionis FD, Gokaslan ZL, Sciubba DM. Surgical management of primary and metastatic spinal tumors. Cancer Control. 2014 Apr;21(2):133-9.
  35. Dea N, Versteeg AL, Sahgal A, Verlaan JJ, Charest-Morin R, Rhines LD, et al. Metastatic Spine Disease: Should Patients With Short Life Expectancy Be Denied Surgical Care? An International Retrospective Cohort Study. Neurosurgery. 2020 Aug;87(2):303-11.
  36. Tabourel G, Terrier LM, Dubory A, Cristini J, Nail LL, Cook AR, et al. Are spine metastasis survival scoring systems outdated and do they underestimate life expectancy? Caution in surgical recommendation guidance. J Neurosurg Spine. 2021 Jul;35(4):527-34.
  37. Lee BH, Kim TH, Chong HS, Moon ES, Park JO, Kim HS, et al. Prognostic factor analysis in patients with metastatic spine disease depending on surgery and conservative treatment: review of 577 cases. Ann Surg Oncol. 2013 Jan;20(1):40-6.
  38. Oka S, Matsumiya H, Shinohara S, Kuwata T, Takenaka M, Chikaishi Y, et al. Total or partial vertebrectomy for lung cancer invading the spine. Ann Med Surg (Lond). 2016 Oct;12:1-4.
  39. Unal S, Feller R, Stadhouder A, Heineman DJ, Jiya TU, van Dorp M, et al. Superior sulcus tumors invading the spine: multimodal treatment outcomes from the preimmunotherapy era. JTO Clin Res Rep [Internet]. 2023 Oct;4(12):100582. Available from: https://pubmed.ncbi.nlm.nih.gov/38046379/
  40. Park SJ, Ma CH, Lee CS, Jeon CY, Shin TS, Park JS. Survival and functional outcomes after surgical treatment for spinal metastasis in patients with a short life expectancy. J Clin Med. 2022 Dec;12(1):46.
  41. Chakravarthy VB, Schachner B, Amin AG, Reiner AS, Yamada Y, Schmitt A, et al. The impact of targetable mutations on clinical outcomes of metastatic epidural spinal cord compression in patients with non-small-cell lung cancer treated with hybrid therapy (Surgery Followed by Stereotactic Body Radiation Therapy). Neurosurgery. 2023 Mar;92(3):557-64.
  42. Zheng J, Ding X, Wu J, Li L, Gao X, Huang Q, et al. Prognostic factors and outcomes of surgical intervention for patients with spinal metastases secondary to lung cancer: An update systematic review and meta analysis. Eur Spine J. 2023 Jan;32(1):228-43.