Is manual palpation of the lung necessary in patients undergoing pulmonary metastasectomy?

Abstract

A best evidence topic in thoracic surgery was written according to a structured protocol. The question addressed was whether manual palpation of the lung is necessary in patients undergoing pulmonary metastasectomy. In total, 56 articles were found using the described search strategy. After screening these articles and their references, 18 publications represented the best evidence to answer the clinical question. No randomized controlled trial addressing the three-part question was available. The authors, journal, date and country of publication, patient group, study type, relevant outcomes and results of these papers were tabulated. The studies reported on 1472 patients with different primary cancers. The patients underwent more than 1630 pulmonary metastasectomies between 1990 and 2014 after the treatment of primary cancer. Almost three quarters of patients underwent open procedures like thoracotomy or sternotomy. Most frequently, helical CT with a slice thickness ranging between 1 and 10 mm was used for preoperative imaging. The sensitivity in detecting pulmonary nodules ranged from 34 to 97%. The corresponding sensitivity rates for PET–CT were 66–67.5 and 75% for high-resolution CT. The positive predictive value for lesions detected by helical CT varied from 47 to 96%. Helical CT reached a specificity between 54 and 93% in detecting pulmonary nodules. The surgeons identified more nodules by meticulous palpation than helical CT. It is noteworthy that up to 48.5% of these palpated nodules were benign lesions (false-positive). Patients with smaller imaged nodules, multiple imaged nodules or primary mesenchymal tumour are more likely to have occult pulmonary nodules. We conclude that not all palpable pulmonary nodules can be imaged preoperatively. Thoracotomy allows the manual palpation of the ipsilateral hemithorax and might be superior to video-assisted thoracic surgery regarding radical resection. However, not all palpable nodules are malignant, and the impact of non-resected pulmonary metastases on patient survival is not clearly evaluated.

INTRODUCTION

A best evidence topic was constructed according to the structured protocol. This protocol is fully described in the ICVTS [1].

THREE-PART QUESTION

In patients undergoing [pulmonary metastasectomy] is [resection of the mass visible on CT] or [resection of the mass and manual palpation of the ipsilateral lung] the best operation [in order to avoid future lung metastases and to optimize survival]?

SCENARIO

You have been asked by the interdisciplinary tumour board to operate on a 73-year old man with oligometastatic colorectal carcinoma. A colorectal resection was performed 5 years ago. There is no cancer evidence apart from one lung metastasis. During pulmonary metastasectomy, your trainee surgeon asks you whether manual palpation is still necessary in an era of modern CT. You are now searching for evidence to answer his question.

SEARCH STRATEGY

The literature research has been performed in Medline and the Cochrane Database of Systematic reviews on 28 July 2015 for articles published since 1 January 2000. The search strategy was (<pulmonary> OR <lung>) AND (<metastasis> OR <metastases> OR <metastatic> OR <metastasectomy> OR <metastatectomy>) AND (<palpation>).

SEARCH OUTCOME

A total of 112 articles in Medline and 0 reviews in the Cochrane Database of Systematic reviews were found. Sixteen were deemed relevant. The screening of references of these articles leads to the inclusion of two additional articles. These 18 articles are listed and summarized in Table 1.

Table 1:

Best evidence papers

Author, date, journal and country Study type (level of evidence)	Patient group	Investigated outcomes	Key results	Comments/study weaknesses
Ambrogi et al. (2000), Ann Thorac Surg, Italy [2] Case series (EbM-level 4)	22 patients Study period: 1995–1999 22 operations Thoracotomy: n = 0 VATS: n = 0 Sternotomy: n = 0 VATS + transxiphoidal approach: n = 22 Mixed primary cancer Number of preoperative PM =1: not reported >1: not reported Radiographic method Single slice helical CT scan 5 mm slice thickness No contrast medium Interval between CT and operation Mean 8 days (range 4–15 days)	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	83.7% 8 PM in 7 patients (31.8%) Not reported 5 nodules 89.1% N = 46 N = 58 N = 9 nodules (15.5%) (bilateral) Transxiphoid approach revealed 12 unexpected contralateral nodules of which 8 were malignant	Evaluation of hard copies of chest CT scan
Loehe et al. (2001), Ann Thorac Surg, Germany [3] Cohort study (EbM-level 2)	63 patients Study period: 1996–1998 71 operations Thoracotomy: n = 71 VATS: n = 0 Sternotomy: n = 0 Other: n = 0 Mixed primary cancer Number of preoperative PM =1: N = 39 >1: N = 32 Radiographic method Helical CT scan 8 mm slice thickness 100% with contrast medium Interval between CT and operation Not reported	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported Not clearly reported Not reported Not clearly reported (N = 1 patient) Not reported Not clearly reported Not clearly reported Not clearly reported Manual palpation leads to the detection of non-imaged nodules in 19 patients (26.8%)	No report on the outcome of detected nodules, in terms of false positive or malignant
Mineo et al. (2001), Arch Surg, Italy [4] Case series (EbM-level 4)	29 patients Study period: 1995–1999 29 operations (mini)Thoracotomy: n = 0 VATS: n = 0 Sternotomy: n = 0 VATS + transxiphoidal approach: n = 29 Mixed primary cancer Number of preoperative PM =1: not reported >1: not reported Radiographic method Single slice helical CT scan 5 mm slice thickness No contrast medium Interval between CT and operation Mean 8 days (range 4–15 days)	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported 11 PM in 9 patients (31%) Not reported Five nodules in 5 patients (17.2%) Not reported N = 54 N = 69 N = 9 nodules (13%) Mean diameter of occult PM: 6.06 ± 2.78 mm (range 3–12 mm)
Margaritora et al. (2002), Eur J Cardiothorac Surg, Italy [5] Case series (EbM-level 4)	166 patients Study period: 1996–2000 Unclear number of operations Thoracotomy: 100% VATS: n = 0 Sternotomy: n = 0 Other: n = 0 Mixed primary cancer Number of preoperative PM =1: not reported >1: not reported Radiographic method Helical CT scan (n = 88) or high-resolution CT scan (n = 78) 5 mm slice thickness No contrast medium Interval between CT and operation Mean 14 days (range 4–26 days)	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	75% (high-resolution CT) or 82% (helical CT) N = 46 (high-resolution CT) or n = 31(helical CT) metastases Not reported Not reported Not reported N = 142 (high-resolution CT) and n = 142 (helical CT) 361 metastases (benign lesion excluded) Not reported Not reported	No information about benign lesions. No report on outcome of detected nodules, in terms of false positive or malignant
Parsons et al. (2004), Ann Thorac Surg, USA [6] Case series (EbM-level 4)	34 patients Study period: 1999–2003 41 operations Thoracotomy: n = 11 VATS: n = 11 Sternotomy: n = 19 Other: n = 0 Mixed primary cancer Number of preoperative PM =1: n = 14 >1: n = 27 Radiographic method Single slice and multislice helical CT scan 5–8 mm slice thickness 100% with contrast medium Interval between CT and operation Median 30 days (range 1–95 days)	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	78% Not reported 63% 29% [95% CI: 20–38%] Not reported N = 97 N = 134 N = 46 (34%) patients Two primary lung cancers detected No statistical significant influence of interval between chest CT scan and operation on sensitivity	Long interval between chest CT scan and operation. Lesions not found by palpation were classified as benign. Inclusion of primary lung cancer lesions in sensitivity analysis
Kayton et al. (2006), J Pediatr Surg, USA [7] Case series (EbM-level 4)	28 patients Study period: 1996–2004 54 operations Thoracotomy: n = 54 VATS: n = 0 Sternotomy: n = 0 Other: n = 0 Primary osteosarcoma Number of preoperative PM =1: not reported >1: not reported Radiographic method Single slice and multislice helical CT scan 5 mm slice thickness No contrast medium Interval between CT and operation Median 20 days (range 1–85 days)	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported N = 19 operations Not reported 15% Not reported N = 183 N = 329 N = 120 nodules (36.5%) Not reported	Interval between chest CT scan and operation >60 days in some patients
Nakajima et al. (2007), Ann Thorac Surg, Japan [8] Case series (EbM-level 4)	102 patients Study period: 1999–2005 122 operations Thoracotomy: n = 30 VATS: n = 79 Sternotomy: n = 13 Other: n = 0 Primary colorectal cancer Number of preoperative PM =1: n = 77 >1: n = 45 Radiographic method Single slice and multislice helical CT scan 5 mm slice thickness 100% with contrast medium Interval between CT and operation Mean 14.9 days	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	91.3% (for lesions >5 mm in diameter) 15 PM in 9 patients Not reported Not reported Not reported N = 219 N = 250 N = 47 nodules (18.8%) Two primary lung cancers detected
Parsons et al. (2007), Ann Thorac Surg, USA [9] Case series (EbM-level 4)	53 patients Study period: 1996–2004 60 operations Thoracotomy: n = 19 VATS: n = 0 Sternotomy: n = 30 Other: n = 11 Mixed primary cancer Number of preoperative PM =1: not reported >1: not reported Radiographic method Single slice and multislice helical CT scan 4–10 mm slice thickness 92.5% with contrast medium Interval between CT and operation Median 26 days (range 0–95 days)	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	60–63% PM in 27 patients Not reported Nodules in 20–21 patients 47–49% N = 168, N = 173 Not reported Not reported Not reported	Interval between chest CT scan and operation >60 days in some patients. No sufficient report on palpation and false-positive results by palpation
Rena et al. (2007), Eur J Surg Oncol, Italy [10] Case series (EbM-level 4)	27 patients Study period: 1990–2003 27 operations Thoracotomy: not reported VATS: not reported Sternotomy: n = 0 Other: n = 0 Primary breast cancer Number of preoperative PM =1: n = 27 >1: n = 0 Radiographic method CT scan, no further information reported Interval between CT and operation Not reported	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported N = 3 PM in 3 patients Not reported Not reported Not reported N = 27 N = 30 Not reported Not reported	Unknown interval between chest CT scan and operation
Fortes et al. (2008), Eur J Cardiothorac Surg, USA [11] Case series (EbM-level 4)	83 patients Study period: 2002–2006 104 operations Thoracotomy: n = 100 VATS: n = 0 Sternotomy: n = 4 Other: n = 0 Mixed primary cancer Number of preoperative PM =1: not reported >1: not reported Radiographic method 100% PET–CT, with F-18 fluoride and 740 MBq of FDG Interval between CT and operation <42 days	Sensitivity (PET–CT) False-negative (PET–CT) Specificity (PET–CT) False-positive (PET–CT) PPV Nodules on PET–CT Palpated nodules False-positive (palpation) Other	67.5% N = 50 nodules Not reported Not reported Not reported N = 104 Not reported Not reported PET–CT sensitivity for nodules >25 mm was 88.5% PET–CT sensitivity for nodules from cholangiosarcoma, adrenocortical carcinoma and Hürthle cell carcinoma was 100%	No report on outcome of detected nodules, in terms of false positive or malignant
Kang et al. (2008), Eur J Cardiothorac Surg, South Korea [12] Cohort study (EbM-level 2)	27 patients Study period: 2005–2006 36 operations Thoracotomy: n = 36 VATS: n = 0 Sternotomy: n = 0 Other: n = 0 Mixed primary cancer, separation between osteosarcoma and non-osteosarcoma patients Number of preoperative PM =1: n = not reported >1: n = not reported Radiographic method 16-detector row CT scan 1 mm slice thickness 100% with contrast medium Interval between CT and operation Not reported	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	34% (osteosarcoma) or 97% (non-osteosarcoma) Not reported 93% (osteosarcoma) or 54% (non-osteosarcoma) Not reported 92% (osteosarcoma) or 64% (non-osteosarcoma) N = 117 N = 198 N = 96 nodules (48.5%) One primary lung cancer detected The size difference between benign lesions and PM was significant [2.4 vs 8.1 mm] The CT scan is inadequate to detect nodules in patients with primary osteosarcoma	Unknown interval between chest CT scan and operation
Pfannschmidt et al. (2008), Thorac Cardiovasc Surg, Germany [13] Case series (EbM-level 4)	93 patients Study period: 2004–2007 125 operations Thoracotomy: n = 125 VATS: n = 0 Sternotomy: n = 0 Other: n = 0 Mixed primary cancer Number of preoperative PM =1: n = not reported >1: n = not reported Radiographic method Four slice and helical CT scan 3–5 mm slice thickness 73.1% with contrast medium Interval between CT and operation Median 12 days (range 1–121 days)	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	83.7 or 88.8% (5 or 3 mm slice thickness) 19.2 or 25.6% (3 or 5 mm slice thickness) Not reported 25.6 or 47.2% (5 or 3 mm slice thickness) 59.4 or 70.7% (5 or 3 mm slice thickness) N = 277 or N = 294 (5 or 3 mm slice thickness) N = 386 N = 54 nodules (14%) One primary lung cancer detected Significantly higher detection rates of PM with a slice thickness of 3 mm compared with 5 mm (P = 0.014)	Interval between chest CT scan and operation >60 days in 15 patients
Cerfolio et al. (2009), Eur J Cardiothorac Surg, USA [14] Case series (EbM-level 4)	57 patients Study period: 2004–2005 57 operations Thoracotomy: n = 57 VATS: n = 0 Sternotomy: n = 0 Other: n = 0 Mixed primary cancer Number of preoperative PM =1: not reported >1: not reported Radiographic method 64-slice helical CT scan 5 mm slice thickness 100% contrast medium Some patients underwent PET–CT Interval between CT and operation <40 days	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported Not reported Not reported Not reported Not reported Not reported Not reported N = 17 (43.6%) Patients with small nodules or multiple nodules were more likely to have occult metastases	Exclusion of central metastasis (compression or infiltration of lobe/segment bronchus) and metastasis ≥5 cm in diameter. No report on outcome of detected nodules, in terms of false positive or malignant
Cerfolio et al. (2011), Ann Thorac Surg, USA [15] Cohort study (EbM-level 2)	152 patients Study period: 2006–2010 152 operations Thoracotomy: n = 152 VATS: n = 0 Sternotomy: n = 0 Other: n = 0 Mixed primary cancer Number of preoperative PM =1: not reported >1: not reported Radiographic method 64 slice helical CT scan 5 mm slice thickness 100% contrast medium 132 patients underwent PET–CT Interval between CT and operation Not reported	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported Not reported Not reported Not reported Not reported Not reported Not reported Not reported 33.6% of patients had non-imaged nodules. 58.8% of these patients had malignant non-imaged nodules Patients with smaller size of the greatest imaged nodule were more likely to have additional occult lesions [1.6 vs 2.3 cm P = 0.04] Patients with multiple imaged nodules were more likely to have additional occult lesions [2.5 vs 1.0 P = 0.06]	Unknown interval between chest CT scan and operation. No report on outcome of detected nodules, in terms of false positive or malignant
Kidner et al. (2012), Arch Surg, USA [16] Case series (EbM-level 4)	170 patients Study period: 1994–2010 190 operations Thoracotomy: unclear VATS: n = 0 Sternotomy: unclear Other: n = 0 All patients had thoracotomy/sternotomy Primary malignant melanoma Number of preoperative PM =1: not reported >1: not reported Radiographic method CT scan, no further information reported Interval between CT and operation ≤30 days	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported Not reported Not reported Not reported Not reported N = 262 Not reported Not reported Bimanual palpation and visual inspection detected additional lesions in 26% of operations Patients with more preoperatively imaged nodules were more likely to have occult nodules [1.2 nodules vs 2 nodules P = 0.001] Patients with smaller diameters of lesions were more likely to have occult nodules [2.2 vs 1.5 cm P = 0.003]	No sufficient information on the number of preoperative PM, radiographic method and operation procedure. No report on the outcome of detected nodules, in terms of false positive or malignant
Althagafi et al. (2014), Asian Cardiovasc Thorac Ann, Saudi Arabia [17] Case series (EbM-level 4)	215 patients Study period: 2001–2011 215 operations Thoracotomy: n = 215 VATS: n = 0 Sternotomy: n = 0 Other: n = 0 Mixed primary cancer Number of preoperative PM =1: not reported >1: no reported Radiographic method Multislice helical CT scan 2.5–5 mm slice thickness Contrast medium: not reported Interval between CT and operation Not reported	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported Not reported Not reported Not reported Not reported N = 493 N = 604 N = 40 patients Patients with mesenchymal tumours were more likely to have occult nodules than those with epithelial tumours [41 vs 29%]	Unknown interval between chest CT scan and operation
Eckardt and Licht (2014), Ann Thorac Surg, Denmark [18] Cohort study (EbM-level 2)	89 patients Study period: 2010–2014 89 operations All operations started as VATS and switched to thoracotomy Mixed primary cancer Number of preoperative PM =1: n = not reported >1: n = not reported Radiographic method multislice CT scan 3–5 mm slice thickness Contrast medium: not reported Interval between CT and operation <42 days	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	Not reported Not reported Not reported Not reported Not reported N = 140 N = 122 (VATS) and n = 189 (thoracotomy) N = 54 nodules (28.6%) Two primary lung cancers detected VATS missed 22 PM and did not allow the palpation of all suspected nodules Missed PM were more likely to be located in the right upper lobe than in other lobes [P = 0.03]	Exclusion of patients with >3 nodules. Evaluation of chest CT scans exclusively by surgeons. Long interval between chest CT scan and operation for some patients
Hao et al. (2014), Sci Rep, China [19] Case series (EbM-level 4)	62 patients Study period: 2001–2012 65 operations Thoracotomy: n = 0 VATS: n = 0 Sternotomy: n = 0 Transxiphoid hand-assisted thoracoscopic surgery: n = 65 Mixed primary cancer Number of preoperative PM =1: n = not reported >1: n = not reported Radiographic method 100% CT scan, no further information reported 69.3% PET–CT, no further information reported Interval between CT and operation Median 13 days (2–52 days)	Sensitivity (CT) False-negative (CT) Specificity (CT) False-positive (CT) PPV Nodules on CT Palpated nodules False-positive (palpation) Other	63% 67 nodules Not reported 5 nodules 96% N = 141 N = 252 N = 69 nodules (27.4%) Sensitivity of PET–CT in detecting PM was 66%

VATS: video-assisted thoracic surgery; CT: computer tomography; PM: pulmonary metastases; PPV: positive predictive value; PET: positron emission tomography; FDG: fluorodeoxyglucose; MBq: megabecquerel.

RESULTS

The 18 studies included report on 1472 patients with lung metastases from different primary cancers [2–19]. The patients underwent more than 1630 pulmonary metastasectomies between 1990 and 2014. More than 70% of operations have been performed via thoracotomy or sternotomy; the remaining surgeons used video-assisted thoracic surgery (VATS) or VATS combined with a transxiphoidal approach.

The interval between preoperative CT and operation, and therefore manual palpation, ranged from 1 to 121 days. The mean interval varied from 8 to 14.9 days and the median interval from 12 to 30 days. Most frequently, helical CT was used. Margaritora et al. [5] compared helical CT with high-resolution CT. The slice thickness used for helical CT ranged between 1 and 10 mm.

The sensitivity of helical CT in detecting pulmonary nodules was 34% in patients with primary osteosarcoma and 60–97% in mixed series or epithelial tumours. Pfannschmidt et al. [13] showed a significant increase in sensitivity by decreasing slice thickness from 5 mm (83.7%) to 3 mm (88.8%) (P = 0.014). High-resolution CT and PET–CT resulted in sensitivity rates of 75 and 66–67.5%, respectively [5, 11, 19]. The positive predictive value for helical CT reached 47–96%. In the worst case, almost half of the pulmonary nodules imaged on CT were benign lesions. The specificity of helical CT was 93% in osteosarcoma patients and 54 or 63% for non-osteosarcoma patients [7, 12]. In fact, more than one-third of all nodules from patients with primary carcinoma were false-positive results on CT.

Several authors have evaluated the factors influencing the risk of non-imaged nodules. Cerfolio et al. [14, 15] demonstrated that patients with smaller lesions were more likely to have occult metastases (1.6 vs 2.3 cm in diameter, P = 0.04). These results are in concordance with the findings by Kidner et al. [16] (1.5 vs 2.2 cm in diameter, P = 0.003). Furthermore, Kidner et al. [16] showed the correlation between the number of metastases and the risk of missed metastases. Patients with a median number of 2 imaged pulmonary nodules were more likely to have occult metastases than those with 1.2 imaged pulmonary nodules (P = 0.001) [16]. Patients with primary mesenchymal tumours were more likely to have occult metastases than those with epithelial tumours (41 vs 29%) [17]. In a case series with osteosarcoma patients, helical CT imaged only 183 nodules, whereas manual palpation found additional 146 nodules [7].

The role of manual palpation is especially reflected by the rate of true-positive and false-negative findings. The studies document a rate of false-positive findings between 13 and 48.5% [3, 4, 6–8, 12–14, 18, 19]. In the worst case, almost half of the palpated and resected lesions were benign [12]. Consequently, the surgeon should consider parenchyma-sparing methods to reduce the damage caused by the potentially unnecessary resection of false-positive nodules. Notably, manual palpation revealed unknown primary lung cancer in 8 cases (0.5%) [6, 8, 12, 13, 18]. The potential detection of occult metastases supports the reservations regarding VATS as a treatment option for pulmonary metastasectomy. Eckardt and Licht [18] created a special setting for their prospective cohort study to compare VATS with thoracotomy in detecting occult metastases. Every operation started with VATS and the surgeon tried to palpate all imaged nodules. Afterwards, a second surgeon entered the operation, converted to thoracotomy and palpated the entire lung. In VATS patients, 22 pulmonary metastases and 45 benign lesions would have remained undetected due to limited palpation.

Currently, there is a lack of evidence regarding the influence of non-resected metastases on survival. Treasure et al. [20, 21] are conducting the active prospective PulMiCC trial addressing this question. In the absence of evidence either way, manual palpation could be recommended in resections with curative intent [22]. The role of bilateral thoracotomy allowing bilateral palpation in case of unilateral imaged pulmonary nodules is still controversial [22]. Owing to the risk of perioperative morbidity due to thoracotomy, careful CT surveillance might be preferable until there is evidence regarding the consequences of non-resected metastases.

CLINICAL BOTTOM LINE

Surgeons consenting patients for pulmonary metastasectomy should discuss with them the fact that despite improvements in imaging, not all palpable pulmonary nodules can be detected preoperatively by modern helical CT. Thoracotomy seems to be superior to VATS, allowing palpation of the ipsilateral lung and there is an increased chance of finding further nodules at surgery by thoracotomy. However, the patients should also be aware that we do not know if this increased detection of very small metastases would improve their outcome, compared with a VATS approach, or indeed compared with conservative treatment.

Conflict of interest: none declared.