Surgical resection for non-small cell lung cancer invading the chest wall: A 12-year experience in a single center

doi:10.21203/rs.3.rs-2375497/v1

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Surgical resection for non-small cell lung cancer invading the chest wall: A 12-year experience in a single center

https://doi.org/10.21203/rs.3.rs-2375497/v1

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Background

Patients with chest wall invasion, which constitute 5-10% of operable non-small cell lung cancer cases, are heterogeneous in terms of factors that may affect the prognosis. We aim to share our experience including the surgical results of patients with non-small cell lung cancer (NSCLC) who underwent chest wall resection and identify the potential factors that may impact the survival.

Methods

The patients who underwent combined chest wall and lung resection due to primary lung cancer invading the chest wall in our center between 2007 and 2019 were reviewed. Variables such as age, tumor size, histological subtype, surgical technique, depth of invasion, the extent of resection, histological subtype, neoadjuvant, and adjuvant treatment status were examined.

Results

254 patients who underwent combined chest wall and lung resection were included in the study. There were 245 men and 9 women. The mean age was 61.0 ± 8.4 years. The overall survival was 70.9 ± 4.6 months, and the 5-year survival rate was 41.5 ± 3.3%. In multivariate analyses, age, the extent of lung resection, the number of resected ribs, invasion depth, and completeness of chest wall resection were independent factors that have an effect on survival.

Conclusions

This study shows that age, the extent of lung and chest wall resection, invasion depth, and completeness of chest wall resection are independent prognostic factors of survival in patients who underwent combined lung and chest wall resection for NSCLC.

Trial registration

Institutional Review Board of the Dr Suat Seren Chest Diseases and Surgery Medical Practice and Research Center (No: E-49109414-604.02.02)

Chest wall invasion

lung cancer

prognosis

surgery

Lung cancer is the leading cause of cancer mortality worldwide and locally advanced disease is present in approximately one-third of patients at the time of diagnosis [1]. Among the cases with locally advanced lung cancer, patients with chest wall invasion in which complete resection is possible have special importance in terms of superior survival characteristics [2]. However, patients with chest wall invasion are a very heterogeneous group and there are many parameters that can affect the prognosis.

In this study, it was aimed to reveal the prognostic factors by examining the cases of non-small cell lung cancer invading the chest wall who underwent concomitant chest wall and lung resection.

Patient selection

This retrospective study was approved by the local ethics committee (No. E-49109414-604.02.02)

Between January 2007 and December 2019 patients who had non-small cell lung cancer (NSCLC) with the invasion of the thoracic wall and who underwent pulmonary resection including lobectomy, bilobectomy, and pneumonectomy were retrospectively analyzed. Patients who underwent surgical resection for Pancoast or primary chest wall tumors were excluded from the study. Patients with no tumoral invasion in pathological examinations, although the tumor was adherent to the chest wall, were also excluded.

Patient characteristics, data of the perioperative and postoperative course, pathological findings, and long-term prognoses were evaluated by review of the hospital records.

Preoperative evaluation

For preoperative pulmonary risk assessment, pulmonary function test and if necessary, lung perfusion scintigraphy, VO2max and cardiopulmonary exercise tests were performed for each patient. Thorax computed tomography (CT), Positron emission tomography (PET-CT), cranial CT/MR and bronchoscopy were performed for all patients before surgery. In the presence of suspicious mediastinal lymph nodes in thorax CT or PET-CT, advanced mediastinal staging was performed with endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) and/or mediastinoscopy. The preoperative mediastinal staging was performed in accordance with the National Comprehensive Cancer Network (NCCN) guidelines. Surgical resection was not planned for patients with N2 nodal metastases detected in the preoperative period.

In some cases, neoadjuvant chemotherapy/radiotherapy/chemoradiotherapy was applied to increase resectability or reduce the extent of resection with the joint decision of the surgical team and the oncologist.

Surgical technique

Muscle sparing posterolateral thoracotomy was performed in all cases except for 2 patients in whom VATS was applied. Although the primary preference is en-bloc resection, extrapleural mobilization of the tumor was performed when the parietal pleura could be easily dissected from the chest wall. The chest wall was resected at a distance of at least 2 cm from the primary tumor. Two-layer prolene mesh, Gore-Tex® Dual Mesh or methyl-methacrylate sandwich graft was used to reconstruct the defect after chest wall resection. The patients were divided into 3 subgroups (1, 1–3, > 3) according to the number of resected ribs.

Pneumonectomy was performed in cases where the tumor exceeded the interlobar fissure or in centrally located tumors where bronchovascular sleeve resection was not possible. One or two hemovac drains were inserted above the prosthetic material in all cases. In addition to the Hemovac drain, 2 chest tubes were placed in the pleural cavity routinely.

According to the pathological examination, the depth of invasion of the tumor was categorized as superficial and deep. Tumors with soft tissue and/or parietal pleura invasion were classified as superficial and rib invasion was classified as deep.

Postoperative follow-up

A postoperative complication was defined as any deviation from the normal postoperative course.

The patients were routinely kept under observation in the intensive care unit until the morning of the first postoperative day. In the preoperative and postoperative period, the diet of the patients was revised and nutritional support with protein-rich supplement was provided to each patient. After the chest tube removal, patients who were in stable condition and enabled self-maintenance of normal daily activities were discharged. All patients had regular follow-up visits 3 months for the first 2 years, then every 6 months up to 5 years.

There was no consistent institutional protocol for locally advanced lung cancer cases in our center. Therefore, the patients in our study were heterogeneous in terms of the treatment protocols applied. While adjuvant chemotherapy was planned for most of the patients, neoadjuvant chemotherapy or chemoradiotherapy was applied to some patients. Neoadjuvant chemotherapy was planned for patients with mediastinal lymph node metastases which were detected in preoperative assessment of mediastinum. Platinum based chemotherapy regimens were planned as an adjuvant therapy for patients who did not receive neoadjuvant chemotherapy. However, in our study, there was a group consisting of patients who refused chemotherapy and patients who could not complete chemotherapy due to tolerance problems. In addition to chemotherapy, adjuvant radiotherapy was also planned for patients with positive resection margin.

Statistical analyzes

SPSS 25.0 (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. Comparations between frequencies in categorical variables were performed with Chi-squared or Fischer’s exact tests. Normality of distribution was tested with the Shapiro-Wilk test. Normally distributed values were expressed as means ± standard deviations (SD). Student’s t-test was used to compare continuous variables.

DFS and OS were estimated using the Kaplan-Meier method. Cox proportional hazards regression analysis was used for investigating the variables that would have an effect on survival. The Log Rank test was used to compare survival distributions. Binary logistic regression analysis was used to investigate the variables that may have an effect on the completeness of surgical resection. Statistical significance was set at P-value < 0.05 (All P values presented were 2-sided).

Between January 2007 and December 2019, a total of 254 patients who underwent concomitant chest wall and lung resection were included in the study. There were 245 men and 9 women, the mean age was 61.0 ± 8.4 years. Among 254 patients, 210 (82.7%) patients underwent lobectomy, 14 (5.5%) patients underwent bilobectomy and 30 (11.8%) patients underwent pneumonectomy. No operative mortality was observed. Postoperative complications were seen in 40 (15.7%) patients. The most common postoperative complications were prolonged air leak (9.5%), pneumonia (3.9%), and respiratory failure (2%).

The mean tumor diameter was 5.5 cm (range, 0.2 to 11 cm). The most common histological type was squamous cell carcinoma (50.8%). The demographic features, surgical and pathological results of the patients are given in Table 1.

Table 1

Patient characteristics
Characteristics	N = 254
Age (years) (mean ± SD)	61.0 ± 8.4
Age group (> 60 years)	140 (55.1%)
Sex (male)	245 (96.5%)
Neoadjuvant therapy	53 (20.9%)
Chemotherapy	39 (15.3%)
Radiotherapy	8 (3.1%)
Chemoradiotherapy	6 (2.4%)
Histology
Squamous cell ca	129 (50.8%)
Adeno ca	100 (39.4%)
Large cell ca	15 (5.9%)
Others*	10 (3.9%)
Extent of lung resection
Lobectomy	210 (82.7%)
Bilobectomy	14 (5.5%)
Pneumonectomy	30 (11.8%)
Type of chest wall resection
En-bloc resection	186 (73.2%)
Resection after extrapleural mobilization	68 (26.8%)
Number of resected ribs
1	27 (10.6%)
2–3	198 (78.0%)
> 3	29 (11.4%)
Postoperative complication	40 (15.7%)
Operative mortality (yes)	17 (6.7%)
Tumor size (cm) (mean ± SD)	5.5 ± 2.1
Invasion depth
Superficial (parietal pleura ± soft tissue)	113 (44.5%)
Deep (rib)	141 (55.5%)
Completeness of resection
Complete (R0)	228 (89.8%)
Incomplete (R1-2)	26 (10.2%)
T
3	211 (83.1%)
4	43 (16.9%)
N
0	207 (81.5%)
1	30 (11.8%)
2	17 (6.7%)
Adjuvant therapy	156 (61.4%)
Chemotherapy	108 (42.5%)
Radiotherapy	22 (8.7%)
Chemoradiotherapy	26 (10.2%)

More than 3 rib resections were required in 29 (11.4%) of the patients and deep invasion rate and mean tumor size was found to be significantly higher in this group (p:0.041, 0.043).

Overall survival was 70.9 ± 4.6 months and overall disease-free survival was 67.9 ± 4.7 months (Fig. 1). 5-year survival rate was %41.5 ± 3.3 and 5-year disease free survival rate was 40.2 ± 3.3%.

According to the pathological examination, the surgical margin was found positive in 26 (10.2%) of the patients, and in this group, overall survival was 33.6 ± 9.9 months.

In univariate analysis, age, histology, the number of resected ribs, invasion depth, completeness of chest wall resection, and presence of systemic therapy were found to be associated with survival (Table 2) (Fig. 2).

Table 2

Kaplan-Maier survival analyses
Variable	Overall survival (months)	p-value
Age (years)		0.004
≤ 60	83.6 ± 6.8
> 60	55.9 ± 5.5
Operation		0.579
Lobectomy-Bilobectomy	70.8 ± 4.9
Pneumonectomy	65.4 ± 13.5
Histology		0.007
Squamous cell ca	54.9 ± 5.6
Adeno ca	81.5 ± 7.4
Type of chest wall resection		0.356
En-bloc	74.1 ± 5.5
Resection after extrapleural mobilization	62.6 ± 8.3
Number of resected ribs		0.032
1	85.0 ± 11.9
2–3	70.3 ± 5.1
> 3	49.4 ± 12.0
Invasion depth		0.005
Superficial (parietal pleura ± soft tissue)	84.6 ± 7.1
Deep (rib)	60.6 ± 5.8
Completeness of resection		0.00
Complete (R0)	75.2 ± 4.9
Incomplete (R1-2)	33.6 ± 9.9
T stage		0.447
3	71.6 ± 4.9
4	65.0 ± 11.2
Nodal status		0.811
N0	69.7 ± 5.0
N1	74.3 ± 13.9
N2	64.6 ± 17.9
Presence of systemic therapy (neoadjuvant or adjuvant)		0.031
No	59.5 ± 7.9
Yes	80.2 ± 5.9

According to the Cox proportional hazards regression analyses, age, the extent of lung resection, the number of resected ribs, and invasion depth and completeness of chest wall resection were independent factors that have an effect on survival (Table 3).

Table 3

Multivariate survival analysis
Variable	p value	Odds ratio	95% CI
Age (≤ 60/>60 years)	0.019	1.53	1.07–2.19
Operation (lobectomy/pneumonectomy)	0.009	1.95	1.18–3.21
Histology (squamous/adeno)	0.144	0.76	0.53–1.09
Type of chest wall resection (en-blok/extrapleural mobilization)	0.168	1.30	0.89–1.90
Number of resected ribs
1	Ref
2–3	0.033	2.05	1.06–3.97
> 3	0.028	2.38	1.09–5.16
Invasion depth(superficial/deep)	0.024	1.49	1.05–2.12
Completeness of resection (complete/incomplete)	0.006	2.01	1.22–3.29
Presence of systemic therapy (neoadjuvant or adjuvant) (no/yes)	0.067	0.714	0.49–1.02
Ref: reference.

In the multivariate analyzes applied, the histological subtype was found to be the independent variable that had an effect on the completeness of the resection (Table 4).

Table 4

Univariate and multivariate analyses of risk factors for incomplete resection
	Univariate analysis			Multivariate analysis
Variables	p value	Odds ratio	95% CI	p value	Odds ratio	95% CI
Age	0.58	0.79	0.53–1.79	0.23	0.57	0.23–1.42
Neoadjuvant therapy	0.83	1.12	0.40–3.13	0.77	0.85	0.28–2.60
Invasion depth	0.063	2.36	0.95–5.83	0.21	1.88	0.71–5.03
Number of resected ribs
1	0.405	ref	ref	ref	ref	ref
2–3	0.715	1.33	0.29–6.04	0.99	0.99	0.19–5.20
> 3	0.279	2.60	0.46–14.73	0.41	2.24	0.33–15.20
Tumor size	0.26	0.63	0.28–1.42	0.12	0.47	0.18–1.22
Histology	0.08	0.42	0.16–1.11	0.045	0.35	0.13–0.98
Cl: Confidence level, Ref: reference.

In the subgroup analyzes performed by excluding N2 positive patients and patients with incomplete resection, no significant difference in survival was found between the groups that received only neoadjuvant and only adjuvant therapy (p:0.63). However, statistically significantly superior survival results were obtained in patients who received neoadjuvant, or adjuvant therapy compared to the group that did not (p:0.031).

In this study, we demonstrated that age, the extension of lung resection, number of resected ribs, depth of invasion, and completeness of the chest wall resection have an impact on survival in patients with primary lung cancer who underwent chest wall resection.

Patients with chest wall invasion due to primary lung cancer are heterogeneous, and the ideal treatment algorithm for these cases is controversial [2–7].

The first case of combined lung and chest wall resection for locally advanced lung cancer belongs to Coleman [8]. The unsatisfactory survival results obtained with surgical resection alone necessitated the addition of chemotherapy/chemoradiotherapy to the treatment.

In the literature, the mean survival time varies between 28-49.3 months and in most studies, age, tumor size, N status, type of chest wall resection (en-block/extrapleural) and depth of invasion have been shown to be associated with survival [2, 4, 10–13].

Magdeleinat et al. [10] reviewed retrospectively clinical records of 201 patients and identified three independent prognostic factors: nodal involvement, depth of parietal invasion, and age.

Elia et al. [5], in their study conducted on 110 patients who underwent concomitant lung and chest wall resection, stated that the main variable that had an effect on survival was the nodal status, and the type of resection (en-block/extrapleural) did not affect survival.

Doddoli et al. [2] analyzed the data of three institutions and found median survival as 19 months, and the overall 5-year survival rate as 30.7% in patients who underwent combined lung and chest wall resection. In the same study, sex, tumor size, and the number of resected ribs were found to be associated with survival.

In our study, young age, lobectomy, R0 resection, the low number of resected ribs, and superficial invasion were found to be good independent prognostic factors however, tumor size (≤ 5 cm vs > 5 cm), nodal status (n0, n1, n2), and type of chest wall resection (en-block vs extrapleural) were not found to be the effect on survival (p values: 0.40, 0.81, 0.36). In the statistical analysis we conducted to explain the effect of the number of resected ribs on survival, it was observed that in the group of patients who had more than 3 ribs resected, the mean tumor size was larger, and the invasion was deeper. However, no relation was found between the number of resected ribs and the completeness of the resection.

Performing chest wall resection after extrapleural mobilization is a controversial issue, and en-bloc resection of the tumor is usually recommended [5, 7, 16]. However, in our study, no significant relationship could be found between resection type and resection completeness and survival in univariate and multivariate analyses. Therefore, in cases where the parietal pleura can be easily dissected from the chest wall, chest wall resection may be preferred after extrapleural mobilization of the tumor.

Nodal status is a well-known prognostic factor for patients with locally advanced lung cancer. The presence of N2 nodal metastases in patients who underwent combined lung and chest wall resection has been found to be an independent poor prognostic factor in various studies [10, 12, 17]. Although the mean overall survival time of N2 positive patients in our study was shorter than N1 and N0 patients, this difference could not reach statistical significance.

The literature data on the comparison of the two major subtypes of non-small cell lung cancer, squamous and adenocarcinomas, in terms of survival characteristics, contain inconsistency. The existence of many variables other than histological type that may affect survival results is thought to be the main reason for this situation. In the study of Caldarella et al. [18] in which age, gender and smoking status were adjusted, no significant survival difference was observed between histological types.

In the study of Pfannschmidt et al. [19] with stage and age-adjusted cases, squamous cell carcinoma showed a significantly superior survival compared to adenocarcinoma.

In the study of Wang et al. [20], adenocarcinoma showed statistically significantly superior survival compared to squamous cell carcinoma at all stages.

In our study, a significant survival advantage in favor of adenocarcinoma was observed in univariate analysis, but no significant effect on survival was found in multivariate analysis (p:0.144, OR: 0.76). In addition, multivariate analysis revealed that squamous cell carcinoma was an independent risk factor for incomplete resection (p: 0.045, OR: 0.35).

Chemotherapy is often preferred as an adjuvant in patients with locally advanced lung cancer invading the chest wall, and radiotherapy is recommended in the presence of residual tumor [21–23]. However, there are also studies suggesting different treatment protocols. In the study of Kawaguchi et al. [24], patients received chemoradiotherapy before surgical resection and the 5-year overall survival rate was found to be 62.6% and 5-year progression free survival rate was found to be 66.0%.

Although adjuvant chemotherapy was frequently preferred in our study, there is also a group of patients who were given neoadjuvant chemotherapy or chemoradiotherapy according to the joint decision of the surgical team and the oncologist. In the subgroup analysis, by excluding patients who received adjuvant radiotherapy due to incomplete resection, and adjuvant chemotherapy due to N2 nodal metastasis, there wasn't detected a significant difference in survival between patients who received neoadjuvant and adjuvant therapy (71.8 ± 14.1 vs 87.9 ± 7.7 months, p:0.63).

This study has potential limitations. Since it is a retrospective study, the data obtained are limited to patient files and hospital records. In our study, a heterogeneous population, including patients who received neoadjuvant or adjuvant therapy, was formed due to the application of different protocols by different oncologists. Although this situation made it difficult to obtain significant statistical results, the number of patients in our study was sufficient to perform subgroup analysis.

Patients who underwent incomplete resection, which were excluded in some studies, were included in our study. Although this situation has the risk of adversely affecting survival analyses, we preferred to design the study method in this way in order to investigate resection completeness as a prognostic factor.

In conclusion, the results of present study highlight several important issues regarding the cases of non-small cell lung cancer invading the chest wall who underwent surgical resection. Age, extent of lung resection, number of resected ribs, depth of invasion and resection completeness were found to be the main variables affecting prognosis. Although its timing is the preference of the oncologist and surgical team, chemotherapy should be a part of the treatment because it positively affects the prognosis.

Non-surgical treatments should be kept in mind in elderly patients who are found to have extensive and deep invasion radiologically and may require pneumonectomy.

CT: Computed tomography

DFS: Disease-free survival

DLCO: Diffusing capacity of the lungs for carbon monoxide

MRI: Magnetic resonance imaging

NCCN: National Comprehensive Cancer Network

NSCLC: Non-small cell lung cancer

OS: Overall survival

PET: Positron emission tomography

VATS: Video-assisted thoracic surgery

VO2max: Maximal oxygen consumption

Ethics approval and consent to participate

This study was approved by the Institutional Review Board (E-49109414-604.02.02). All methods were performed in accordance with the relevant guidelines and regulations (Declaration of Helsinki). Informed consent was obtained from patients for study participation.

Consent for publication

Not Applicable.

Availability of data and materials

The data underlying this article cannot be shared publicly due to the privacy of individuals that participated in the study. The data will be shared on reasonable request to the corresponding author.

Competing interests

The authors declare that there isn’t any conflict of interest.

Funding

The authors received no specific funding for this work.

Authors' contributions

GB: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Supervision; Writing—review & editing.

AU: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; supervision; Writing—original draft; Writing—review & editing.

SY: Conceptualization; Methodology; Project administration; Writing—original

draft; Writing—review & editing.

KCC: Conceptualization; Data curation; Investigation; Methodology; Project administration; Writing—original draft; Writing—review & editing.

SG: Investigation; Methodology; Writing—review & editing.

SOK: Conceptualization; Investigation; Methodology; Project administration; Writing—original draft; Writing—review & editing.

Acknowledgements

None.

Clinical registration number

Institutional Review Board of the Dr Suat Seren Chest Diseases and Surgery Medical Practice and Research Center

No: E-49109414-604.02.02

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No competing interests reported.

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Surgical resection for non-small cell lung cancer invading the chest wall: A 12-year experience in a single center

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