Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Evaluation of Video-Assisted Thoracoscopic Surgery for Pulmonary Metastases: A Meta-Analysis

  • Siyuan Dong,

    Affiliation Department of Thoracic Surgery, First Hospital of China Medical University, Shenyang, Liaoning Province, People's Republic of China

  • Lin Zhang ,

    zhanglincmu@163.com

    Affiliation Department of Thoracic Surgery, First Hospital of China Medical University, Shenyang, Liaoning Province, People's Republic of China

  • Wenya Li,

    Affiliation Department of Thoracic Surgery, First Hospital of China Medical University, Shenyang, Liaoning Province, People's Republic of China

  • Jiang Du,

    Affiliation Department of Thoracic Surgery, First Hospital of China Medical University, Shenyang, Liaoning Province, People's Republic of China

  • Xiangli Liu,

    Affiliation Department of Thoracic Surgery, First Hospital of China Medical University, Shenyang, Liaoning Province, People's Republic of China

  • Xitao Chen

    Affiliation Department of Thoracic Surgery, First Hospital of China Medical University, Shenyang, Liaoning Province, People's Republic of China

Evaluation of Video-Assisted Thoracoscopic Surgery for Pulmonary Metastases: A Meta-Analysis

  • Siyuan Dong, 
  • Lin Zhang, 
  • Wenya Li, 
  • Jiang Du, 
  • Xiangli Liu, 
  • Xitao Chen
PLOS
x

Abstract

Background

To evaluate the evidence comparing video-assisted thoracic surgery (VATS) and open thoracotomy in the treatment of metastatic lung cancer using meta-analytical techniques.

Methods

A literature search was undertaken until July 2013 to identify the comparative studies evaluating disease-free survival rates and survival rates. The pooled odds ratios (OR) and the 95% confidence intervals (95% CI) were calculated with the fixed or random effect models.

Results

Six retrospective studies were included in our meta-analysis. These studies included a total of 546 patients: 235 patients were treated with VATS, and 311 patients were treated with open thoracotomy. The VATS and the thoracotomy did not demonstrate a significant difference in the 1-,3-,5-year survival rates and the 1-year disease-free survival rate. There were significant statistical differences between the 3-year disease free survival rate (p = 0.04), which favored open thoracotomy.

Conclusions

The VATS approach is a safe and feasible treatment in terms of the survival rate for metastatic lung cancer compared with the thoracotomy. The 3-year disease-free survival rate in the VATS group is inferior to that of open thoracotomy. The VATS approach could not completely replace open thoracotomy.

Introduction

Metastasectomy is considered a beneficial treatment for a patient with metastatic lung cancer whose primary tumor has been well controlled[1].After surgery, 5-year survival rates of 30% to 50% could be achieved depending on the underlying primary cancer[2][4].In practice, the surgical approaches to pulmonary metastases are variable. Video-assisted thoracoscopic surgery (VATS) is an emerging technique; many procedures that had previously required a thoracotomy have been performed with the minimally invasive VATS. VATS has been used for the treatment of pulmonary metastases.

The routine use of VATS for the treatment of respectable metastatic lung cancer remains controversial. Critics of the VATS approach have argued that it might not be an equivalent oncological operation[5], [6]. A prospective study by Cerfolio[7]found that 22% of the nodules that could be detected by thoracotomy were missing by VATS.Whether the VATS approach can provide a satisfactory outcome is unknown.

An evidenced-based investigation of the VATS approach is needed, we undertook this meta-analysis to achieve a more objective assessment of the published studies and to provide a more accurate comparison between VATS and thoracotomy for metastatic lung cancer.

Methods

Search Strategy

Electronic searches were of the MEDLINE,Cochrane Controlled Trial Register (CENTRAL), Ovid MEDILINE, PubMed and Embase databases were performed until July 2013.The following MeSH search headings were used: “metastatic lung cancer”, “pulmonary metastases” “video-assisted thoracic surgery”, “thoracotomy” and “comparative study”.We searched the reference lists of relevant studies, reviews, editorials, letters,and meeting abstracts. We used the Science Citation Index to cross-reference for further studies that met our criteria.

Study Selection

The studies included in this meta-analysis were based on our predetermined criteria as follows: (1) clinical trials that include the full text of the paper published in peer-reviewed English journals or reports of presentations at major thoracic surgery meetings; (2) comparison of the efficacy of VATS to that of thoracotomy in patients with metastatic lung cancer; and (3) similarity in the patients' baseline characteristics.

Data extraction and quality assessment

Two independent reviewers (Siyuan and Wenya) assessed the quality and the risk of bias of the included trials as follows: (1) the studies that did not include a comparative group with surgery as a form of intervention were excluded; (2) the trials focusing on patients undergoing surgery for primary lung cancer were excluded; (3) the studies on robotic video-assisted thoracic surgery were excluded; (4) if there was an overlap between authors, centers or patient cohorts evaluated in the published literature, only the most recent report was included; (5) studies published more than 20 years ago were excluded because of the significant technological changes that has occurred. The articles were evaluated with the Downs and Black quality assessment method[8]. Discrepancies between the two investigators were resolved by discussion and consensus with a senior investigator. The final results were reviewed by two senior investigators (Lin and Jiang).The disease-free survival was defined as the date of the initial metastasectomy until the date of a recurrence.

Statistical and sensitivity analyses

The meta-analysis was performed using the RevMan 5.1.0. software package. The odds ratio (OR) or the mean difference with 95% confidence intervals (95% CI) was calculated for the dichotomous outcomes and the continuous outcomes, respectively. A P value<0.05 was considered a significant difference in the value between the two groups. We used the I2 statistic to investigate the heterogeneity among the studies.The heterogeneity was explored by X2 and I2; I2<25% and I2>50% reflect a small and large inconsistency, respectively. P<0.05 was considered significant. If there were a statistical difference in terms of the heterogeneity (P≤0.05), a random-effect model was selected to pool the data. Otherwise, a fixed-effect model was used. Taking into account the presence of different sample sizes of the included studies, a sensitivity analysis was performed to compare the of 1-year survival rate and the 3-year disease free survival rate between VATS and open thoracotomy.

Publication bias

A funnel plot was used to explore bias. Asymmetry in the funnel plot of trial size against treatment effect was used to assess the risk of bias.

Results

Description of the studies

Six retrospective cohort studies the met our criteria were included in this meta-analysis. A total of 546 patients were included in the six studies;235 patients were allocated to the VATS group, whereas 311 were allocated to the open thoracotomy group to evaluate their survival rate.The search algorithm, results of the search strategies and selection criteria are shown in Fig 1. The patient characteristics and evaluation index are shown in Table 1.

Assessment of Recurrence and Survival

Six studies documented the 1-year survival rate,and there was no significant heterogeneity among the six studies (x2 = 3.79, P = 0.58,I2 = 0%).A fixed effect model was used.The combined result is shown in Fig 2(OR = 1.15; 95%CI, 0.72–1.84; p = 0.58). Because of the heterogeneity in sample size, the sensitivity analyses were conducted using larger sample sizes. There was no difference between the two surgical methods with an OR of 1.00(95%CI 0.55–1.79) and with heterogeneity(Χ2 = 3.23,P = 0.07, I2 = 69%). Five studies reported the 3-year survival rate, and heterogeneity was identified through the five studies (x2 = 11.32,P = 0.02,I2 = 65%); and a random effect model was adopted (OR = 1.07; 95%CI, 0.50–2.27; p = 0.86) (Fig 3). Three studies compared the 5-year survival rate (OR = 0.96; 95%CI, 0.34–2.71; p = 0.93), with certain heterogeneity(x2 = 8.86,P = 0.01,I2 = 77%) (Fig 4).

thumbnail
Figure 2. 1-year survival rate.

Forest plot of the Odds Ratio(OR) of the 1-year survival rate following VATS versus open thoracotomy for metastatic lung cancer.The estimate of the OR of each individual trial corresponds to the middle of the squares and horizontal line gives the 95% CI.On each line,the numbers of events as a fraction of the total number randomized are shown for both treatment groups.For each subgroup,the sum of the statistics, along with the summary OR is represented by the middle of the solid diamonds.A test of heterogeneity between the trials within a subgroup is given below the summary statistics.

https://doi.org/10.1371/journal.pone.0085329.g002

thumbnail
Figure 3. 3-year survival rate.

Forest plot of the Odds Ratio(OR) of the 3-year survival rate following VATS versus open thoracotomy for metastatic lung cancer.The estimate of the OR of each individual trial corresponds to the middle of the squares and horizontal line gives the 95% CI.On each line,the numbers of events as a fraction of the total number randomized are shown for both treatment groups.For each subgroup,the sum of the statistics, along with the summary OR is represented by the middle of the solid diamonds.A test of heterogeneity between the trials within a subgroup is given below the summary statistics.

https://doi.org/10.1371/journal.pone.0085329.g003

thumbnail
Figure 4. 5-year survival rate.

Forest plot of the Odds Ratio(OR) of the 5-year survival rate following VATS versus open thoracotomy for metastatic lung cancer.The estimate of the OR of each individual trial corresponds to the middle of the squares and horizontal line gives the 95% CI.On each line,the numbers of events as a fraction of the total number randomized are shown for both treatment groups.For each subgroup,the sum of the statistics, along with the summary OR is represented by the middle of the solid diamonds.A test of heterogeneity between the trials within a subgroup is given below the summary statistics.

https://doi.org/10.1371/journal.pone.0085329.g004

Four studies compared the 1-year disease free survival rate (OR = 1.31; 95% CI, 0.79–2.19; p = 0.30),finding no significant heterogeneity among these studies (x2 = 1.82,P = 0.61,I2 = 0%) (Fig 5), and four studies compared the 3-year disease free survival rate (OR = 0.59; 95% CI,0.38–0.91; p = 0.02), finding no significant heterogeneity (x2 = 1.82,P = 0.61,I2 = 0%) between the patients who underwent VATS and those who underwent open thoracotomy (Fig 6). Because of the heterogeneity in the sample size, sensitivity analyses were conducted using larger sample size studies; however, there was no difference between the two surgical methods with an OR of 1.71 (95% CI,1.02–2.89) and with heterogeneity (Χ2 =  3.07,P  = 0.22, I2 = 35%). There were significant 3-year disease free survival rate benefits with open thoracotomy. We attempted to evaluate the 5-year disease free survival rate.Only two studies reported these rates,and the published data were not sufficient for the combined analysis.

thumbnail
Figure 5. 1-year disease-free survival rate.

Forest plot of the Odds Ratio(OR) of the 1-year disease free survival rate following VATS versus open thoracotomy for metastatic lung cancer.The estimate of the OR of each individual trial corresponds to the middle of the squares and horizontal line gives the 95% CI.On each line,the numbers of events as a fraction of the total number randomized are shown for both treatment groups.For each subgroup,the sum of the statistics, along with the summary OR is represented by the middle of the solid diamonds.A test of heterogeneity between the trials within a subgroup is given below the summary statistics.

https://doi.org/10.1371/journal.pone.0085329.g005

thumbnail
Figure 6. 3-year disease-free survival rate.

Forest plot of the Odds Ratio(OR) of the 3-year survival rate following VATS versus open thoracotomy for metastatic lung cancer.The estimate of the OR of each individual trial corresponds to the middle of the squares and horizontal line gives the 95% CI.On each line,the numbers of events as a fraction of the total number randomized are shown for both treatment groups.For each subgroup,the sum of the statistics, along with the summary OR is represented by the middle of the solid diamonds.A test of heterogeneity between the trials within a subgroup is given below the summary statistics.

https://doi.org/10.1371/journal.pone.0085329.g006

Publication bias

Publication bias might exist when nonsignificant findings remain unpublished,thus artificially inflating the apparent magnitude of an effect.The funnel plots of the study are shown in Figure 7.The funnel plots of the 1-year survival rate following VATS and thoracotomy for the treatment of metastatic lung cancer showed asymmetry, which suggested that there was some publication bias.

Discussion

Many tumors can metastasize to the lung,and colorectal and breast tumors are the most common primary tumors[9].Pulmonary resection has been shown to be beneficial for patients with resectable and isolated pulmonary metastases[10]. Traditional open thoracotomy and VATS are two principally different surgical methods for pulmonary metastasectomy.The selection of an approach depends more on the theoretical knowledge and personal experience of the surgeon than on the evidence. Over the past two decades, several studies have demonstrated the benefits of VATS that included less postoperative pain, shorter hospital stays, a smaller degree of immunosuppression and enhanced recovery and the ability to tolerate adjuvant therapy[11][13]. Whether the long-term advantages are comparable to those of open thoracotomy is not well documented.

The major deficiency of the VATS approach is that nodules might be undetected by VATS that might be detected by manual palpation during thoracotomy; such missing nodules are not imaged on a preoperative CT scan. The VATS approach has long been controversial because VATS does not consistently detect all the metastases, and it is recognized that complete resection remains a major determining factor of survival [14].The detection rate of HRCT for pulmonary metastases is 78–84%[15][17].Kayton[18]found that 35% of the pathologically verified metastases were missed by CT. In the International Registry of Lung Metastases study of 5206 patients, the 5-year survival rate was 36% for complete resection compared with 13% incomplete resectoin[19]. It is not certain whether the nodule imaged on a CT scan and resected by VATS is the correct one [14]. Those who disagree with the use of VATS hypothesize that VATS-related recurrence is commonly observed, including port-site recurrence and resection stump recurrence[20]. Johnstone reported 23 cases of port-site chest wall recurrence related to VATS[21]. They hypothesized that the thoracoscopic approach should only be used in patients with a solitary lesion and when resection is requried for diagnostic purposes.

The surgeons who favor the VATS approach advocate that VATS minimizes pain and trauma to the patients and that the VATS group might have an improved tolerance of chemotherapy, which would likely ensure delivery of planned post-resection adjuvant therapy without a reduction in dosage or delay. The standard surgical procedure for pulmonary metastases is wedge resection that usually does not require manipulation of the pulmonary hilum, which is appropriate for the VATS approach.They hypothesiezd that a lesion overlooked by CT but detected by palpation might not result in a survival gain[22], [23], and may be partially compensated for by carefully follow-up.Flores[24] hypothesized that the VATS group might demonstrate a great number of metachronous tumors over time;however, the metachronous lesions in each group was similar.

Our work suggests that thoracoscopic resection of metastatic lung cancer is a safe and curative procedure with 1, 3, and 5-year survival rates comparable to those of thoracotomy. Patients with metastatic lung cancer are likely to relapse in the lung, and after lung metastasectomy by VATS, patients might benefit from a second metastasectomy. We hypothesize that earlier chemotherapy and radiation are essential to maximizing survival. Our study might be subject to pretreatment selection bias, because most of the patients selected for open thoracotomy had multiple lesions and high risk and were not suitable for treatment with VATS.The missing lesions perhaps skewed the data more toward VATS as an equivalent procedure.

We were also interested in the recurrence of cancer,and the disease-free survival rates were evaluated. This study demonstrates a similar 1-year disease-free survival rate;however, the 3-year disease-free survival rate is inferior for three reasons. First, unrelated cancer deaths were included in our analysis of the 1, 3, and 5-year overall survival, which might account for VATS having a comparable overall survival rate but an inferior disease-free survival rate. Second,the patients in the VATS group might have lesions that are missed and there are more likely to relapse in the lung, leading to the inferior 3-year disease-free survival rate.Third, some of our included studies were in the early period of VATS development when the technology was immature, and some of the complications can now be prevented with more experience. Schaeff[25] reported 23 cases of port-site recurrence associated with VATS that occurred before 1998.The number of cases studied was small, and the observation period was limitied.

Spiral computed tomography has a far higher detection rate today than it did 20 years ago;so small lesions can be accurately localized before surgery[26], which ensures the success of VATS. With advances in imaging technology, palpaiton during open thoracotomy is becoming less important.The latest VATS technology has a high-definition resolution and the flexible-tip thoracoscope enables complete inspection of the pleural cavity.These advancements ensure that VATS is an ideal method for patients with a solitary and relatively small peripheral lesions.Tamas[27] hypothesizes that palpation is necessary in a therapeutic metastasectomy as opposed to a diagnostic procedure.Whether patients with multiple lesions should be treated with open thoracotomy or VATS is controversial.

This study is the first meta-analysis of the oncological outcome of thoracoscopic surgery for the treatment of metastatic lung cancer. In our work, we observed that VATS might be a promising treatment for metastatic lung cancer. No randomized trials existing to guide doctors in the field of metastatic lung cancer currently. A prospective randomized study of the different surgical strategies is needed.

Limitation

No randomized controlled trials existing to comparing VATS with thoracotomy have been conducted. Heterogeneity was observed between the sample size and the years covered. Most studies are limited to small observational studies and single-institution case series. For these reasons,there are only a total of 546 patients were included in the two groups, for a study period spans more than a decade. Two of the studies comprise almost 65% of the patients, and one study has only 20 patients; there are potential sources of bias in our work.Additional randomized controlled trials in the studies we accessed would have increased the strength of our results.There is a bias for the English language.

Conclusion

In our meta-analysis we found that for patients with metastatic lung cancer, comparing VATS with thoracotomy showed almost equivalent survival rates. The VATS can not replace open thoracotomy completely. Further study is needed,and a large multicenter randomized trial comparing VATS and thoracotomy would be ideal.

Supporting Information

Author Contributions

Conceived and designed the experiments: SYD LZ. Performed the experiments: SYD LZ WYL JD XLL XTC. Analyzed the data: SYD LZ WYL JD XLL XTC. Contributed reagents/materials/analysis tools: SYD LZ WYL JD XLL XTC. Wrote the paper: SYD LZ.

References

  1. 1. Rusch VW (2010) Pulmonary metastasectomy: a moving target. J Thorac Oncol 5: S130–131.
  2. 2. Casson AG, Putnam JB, Natarajan G, Johnston DA, Mountain C, et al. (1992) Five-year survival after pulmonary metastasectomy for adult soft tissue sarcoma. Cancer 69: 662–668.
  3. 3. van Halteren HK, van Geel AN, Hart AA, Zoetmulder FA (1995) Pulmonary resection for metastases of colorectal origin. Chest 107: 1526–1531.
  4. 4. Kandioler D, Kromer E, Tuchler H, End A, Muller MR, et al. (1998) Long-term results after repeated surgical removal of pulmonary metastases. Ann Thorac Surg 65: 909–912.
  5. 5. McCormack PM, Bains MS, Begg CB, Burt ME, Downey RJ, et al. (1996) Role of video-assisted thoracic surgery in the treatment of pulmonary metastases: results of a prospective trial. Ann Thorac Surg 62: 213–216 discussion 216–217.
  6. 6. Saisho S, Nakata M, Sawada S, Yamashita M, Saeki H, et al. (2009) Evaluation of video-assisted thoracoscopic surgery for pulmonary metastases: 11-years of experience. Surg Endosc 23: 55–61.
  7. 7. Cerfolio RJ, Bryant AS, McCarty TP, Minnich DJ (2011) A prospective study to determine the incidence of non-imaged malignant pulmonary nodules in patients who undergo metastasectomy by thoracotomy with lung palpation. Ann Thorac Surg 91: 1696–1700 discussion 1700–1691.
  8. 8. Downs SH, Black N (1998) The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health 52: 377–384.
  9. 9. Kondo H, Okumura T, Ohde Y, Nakagawa K (2005) Surgical treatment for metastatic malignancies. Pulmonary metastasis: indications and outcomes. Int J Clin Oncol 10: 81–85.
  10. 10. Porter GA, Cantor SB, Walsh GL, Rusch VW, Leung DH, et al. (2004) Cost-effectiveness of pulmonary resection and systemic chemotherapy in the management of metastatic soft tissue sarcoma: a combined analysis from the University of Texas M. D. Anderson and Memorial Sloan-Kettering Cancer Centers. J Thorac Cardiovasc Surg 127: 1366–1372.
  11. 11. Petersen RP, Pham D, Burfeind WR, Hanish SI, Toloza EM, et al. (2007) Thoracoscopic lobectomy facilitates the delivery of chemotherapy after resection for lung cancer. Ann Thorac Surg 83: 1245–1249 discussion 1250.
  12. 12. Paul S, Altorki NK, Sheng S, Lee PC, Harpole DH, et al. (2010) Thoracoscopic lobectomy is associated with lower morbidity than open lobectomy: a propensity-matched analysis from the STS database. J Thorac Cardiovasc Surg 139: 366–378.
  13. 13. Whitson BA, Groth SS, Duval SJ, Swanson SJ, Maddaus MA (2008) Surgery for early-stage non-small cell lung cancer: a systematic review of the video-assisted thoracoscopic surgery versus thoracotomy approaches to lobectomy. Ann Thorac Surg 86: 2008–2016 discussion 2016–2008.
  14. 14. Eckardt J, Licht PB (2012) Thoracoscopic versus open pulmonary metastasectomy: a prospective, sequentially controlled study. Chest 142: 1598–1602.
  15. 15. Ambrogi V, Paci M, Pompeo E, Mineo TC (2000) Transxiphoid video-assisted pulmonary metastasectomy: relevance of helical computed tomography occult lesions. Ann Thorac Surg 70: 1847–1852.
  16. 16. Margaritora S, Porziella V, D'Andrilli A, Cesario A, Galetta D, et al. (2002) Pulmonary metastases: can accurate radiological evaluation avoid thoracotomic approach? Eur J Cardiothorac Surg 21: 1111–1114.
  17. 17. Parsons AM, Detterbeck FC, Parker LA (2004) Accuracy of helical CT in the detection of pulmonary metastases: is intraoperative palpation still necessary? Ann Thorac Surg 78: 1910–1916 discussion 1916–1918.
  18. 18. Kayton ML, Huvos AG, Casher J, Abramson SJ, Rosen NS, et al. (2006) Computed tomographic scan of the chest underestimates the number of metastatic lesions in osteosarcoma. J Pediatr Surg 41: 200–206 discussion 200–206.
  19. 19. Long-term results of lung metastasectomy: prognostic analyses based on 5206 cases. The International Registry of Lung Metastases. J Thorac Cardiovasc Surg 113: 37–49.
  20. 20. Mutsaerts EL, Zoetmulder FA, Rutgers EJ (2001) Port site metastasis as a complication of thoracoscopic metastatectomy. Eur J Surg Oncol 27: 327–328.
  21. 21. Johnstone PA, Rohde DC, Swartz SE, Fetter JE, Wexner SD (1996) Port site recurrences after laparoscopic and thoracoscopic procedures in malignancy. J Clin Oncol 14: 1950–1956.
  22. 22. Treasure T (2007) Pulmonary metastasectomy: a common practice based on weak evidence. Ann R Coll Surg Engl 89: 744–748.
  23. 23. Roth JA, Pass HI, Wesley MN, White D, Putnam JB, et al. (1986) Comparison of median sternotomy and thoracotomy for resection of pulmonary metastases in patients with adult soft-tissue sarcomas. Ann Thorac Surg 42: 134–138.
  24. 24. Flores RM, Ihekweazu UN, Rizk N, Dycoco J, Bains MS, et al. (2011) Patterns of recurrence and incidence of second primary tumors after lobectomy by means of video-assisted thoracoscopic surgery (VATS) versus thoracotomy for lung cancer. J Thorac Cardiovasc Surg 141: 59–64.
  25. 25. Schaeff B, Paolucci V, Thomopoulos J (1998) Port site recurrences after laparoscopic surgery. A review. Dig Surg 15: 124–134.
  26. 26. Chen YR, Yeow KM, Lee JY, Su IH, Chu SY, et al. (2007) CT-guided hook wire localization of subpleural lung lesions for video-assisted thoracoscopic surgery (VATS). J Formos Med Assoc 106: 911–918.
  27. 27. Molnar TF, Gebitekin C, Turna A (2010) What are the considerations in the surgical approach in pulmonary metastasectomy? J Thorac Oncol 5: S140–144.
  28. 28. Nakajima J, Takamoto S, Tanaka M, Takeuchi E, Murakawa T, et al. (2001) Thoracoscopic surgery and conventional open thoracotomy in metastatic lung cancer. Surg Endosc 15: 849–853.
  29. 29. Mutsaerts EL, Zoetmulder FA, Meijer S, Baas P, Hart AA, et al. (2002) Long term survival of thoracoscopic metastasectomy vs metastasectomy by thoracotomy in patients with a solitary pulmonary lesion. Eur J Surg Oncol 28: 864–868.
  30. 30. Nakas A, Klimatsidas MN, Entwisle J, Martin-Ucar AE, Waller DA (2009) Video-assisted versus open pulmonary metastasectomy: the surgeon's finger or the radiologist's eye? Eur J Cardiothorac Surg 36: 469–474.
  31. 31. Carballo M, Maish MS, Jaroszewski DE, Holmes CE (2009) Video-assisted thoracic surgery (VATS) as a safe alternative for the resection of pulmonary metastases: a retrospective cohort study. J Cardiothorac Surg 4: 13.
  32. 32. Gossot D, Radu C, Girard P, Le Cesne A, Bonvalot S, et al. (2009) Resection of pulmonary metastases from sarcoma: can some patients benefit from a less invasive approach? Ann Thorac Surg 87: 238–243.
  33. 33. Chao YK, Chang HC, Wu YC, Liu YH, Hsieh MJ, et al. (2012) Management of lung metastases from colorectal cancer: video-assisted thoracoscopic surgery versus thoracotomy—a case-matched study. Thorac Cardiovasc Surg 60: 398–404.