EUROPEAN RESPIRATORY REVIEW

REVIEW
C. AIGNER ET AL.

Resectable non-stage IV nonsmall cell lung cancer: the surgical

perspective
1
Clemens Aigner , Hasan Batirel 2, Rudolf M. Huber 3
, David R. Jones 4
, Alan D.L. Sihoe 5
,
Tomaž Štupnik 6
and Alessandro Brunelli 7

1
Department of Thoracic Surgery, Medical University of Vienna, Vienna, Austria. 2Department of Thoracic Surgery, Marmara University,
Istanbul, Turkey. 3Division of Respiratory Medicine and Thoracic Oncology, and Thoracic Oncology Centre Munich, Ludwig-Maximilians-
Universität in Munich, Munich, Germany. 4Department of Thoracic Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY,
USA. 5Department of Cardio-Thoracic Surgery, CUHK Medical Centre, Hong Kong, China. 6Department of Thoracic Surgery, Ljubljana
University Medical Centre, Ljubljana, Slovenia. 7Department of Thoracic Surgery, St James’s University Hospital, Leeds, UK.

Corresponding author: Alessandro Brunelli (brunellialex@gmail.com)

Shareable abstract (@ERSpublications)

Surgery represents a key element in the multidisciplinary management of lung cancer. Surgical
aspects such as operability, resectability, surgical access and extent of resection are important and
should be learned by all nonsurgical members of the MDT. https://bit.ly/41WDYmx

Cite this article as: Aigner C, Batirel H, Huber RM, et al. Resectable non-stage IV nonsmall cell lung
cancer: the surgical perspective. Eur Respir Rev 2024; 33: 230195 [DOI: 10.1183/16000617.0195-2023].

Copyright ©The authors 2024
This version is distributed under
the terms of the Creative
Commons Attribution
Non-Commercial Licence 4.0.
For commercial reproduction
rights and permissions contact
permissions@ersnet.org
Received: 9 Oct 2023
Accepted: 11 Jan 2024
Abstract
Surgery remains an essential element of the multimodality radical treatment of patients with early-stage
nonsmall cell lung cancer. In addition, thoracic surgery is one of the key specialties involved in the lung
cancer tumour board. The importance of the surgeon in the setting of a multidisciplinary panel is ever-
increasing in light of the crucial concept of resectability, which is at the base of patient selection for
neoadjuvant/adjuvant treatments within trials and in real-world practice. This review covers some of the
topics which are relevant in the daily practice of a thoracic oncological surgeon and should also be known
by the nonsurgical members of the tumour board. It covers the following topics: the pre-operative selection
of the surgical candidate in terms of fitness in light of the ever-improving nonsurgical treatment
alternatives unfit patients may benefit from; the definition of resectability, which is so important to include
patients into trials and to select the most appropriate radical treatment; the impact of surgical access and
surgical extension with the evolving role of minimally invasive surgery, sublobar resections and
parenchymal-sparing sleeve resections to avoid pneumonectomy.

Introduction
Surgery remains an essential element of the multimodality radical treatment of patients with early-stage
nonsmall cell lung cancer (NSCLC). As a consequence, the surgeon is one of the essential members in the
tumour board. Their importance in the setting of a multidisciplinary panel is ever-increasing in light of the
crucial concept of resectability, which is at the base of patient selection for neoadjuvant/adjuvant treatments.

In this review we will cover some of the topics which are relevant in the daily practice of a thoracic
surgeon and should also be known by the nonsurgical members of the tumour board: the pre-operative
fitness evaluation of the surgical candidate in light of the ever-improving nonsurgical treatment alternatives
unfit patients may benefit from; the definition of resectability which is critical to select the most
appropriate radical treatment; and the impact of the surgical access and surgical extension with the
evolving role of minimally invasive surgery (MIS), sublobar resections and parenchymal-sparing sleeve
resections to avoid pneumonectomy.

Methods
Search strategy
The search strategy was as follows: original talks addressing the subject from the Collaborative Course of
the European Society of Thoracic Surgeons (ESTS) and the European Respiratory Society (ERS) on

https://doi.org/10.1183/16000617.0195-2023 Eur Respir Rev 2024; 33: 230195

EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

Thoracic Oncology held in Zurich (February 2023) and their relevant references were included. Additional
searches for each of the subtopics included in this narrative review were conducted to retrieve relevant
publications which were not discussed during the presentation at the aforementioned meeting.
Peer-reviewed studies in English from January 1990 to June 2023 from PubMed and MEDLINE databases
were evaluated with regard to the immediate affinity of the published papers to the original talks. Letters to
the Editor, congress abstracts and case reports were excluded.

It is not our aim to provide an extensive and systematic review of the topics presented here. Instead, this
review aims to further our understanding of the most recent expert opinion and related evidence in
pre-operative selection of the surgical candidate, definition of resectability, impact of the surgical access on
outcome, and parenchymal-sparing resections for early-stage and more locally advanced-stage lung cancer.

Pre-operative risk assessment of the surgical candidate

Early and localised NSCLC is a heterogenous potentially curable group with various tumour stages,
biology and varying prognosis. Treatment options range from segmentectomy in early lung cancer to
radiotherapy plus systemic therapy in a multimodality setting in more advanced disease. To improve
oncological outcome, patients are often treated with various treatment modalities. Their toxicities and
functional impairments can overlap and be increased.

Comorbidities and risks in lung cancer patients

Major issues can be bronchopulmonary and cardiovascular as well as liver, renal and neurological diseases,
diabetes and alterations of the immune system [1–3]. Scarce evidence regarding consequences can be
found for many comorbidities; however, there are specific recommendations for COPD and cardiovascular
diseases.

For interstitial lung diseases (ILDs), literature mostly from Asia describes increased surgical complications,
mostly pulmonary adverse events, and early deaths [4–6]. Also, for stereotactic and conventional
radiotherapy, increased pulmonary complications are reported [7–9]. Acute ILD exacerbations have a high
risk of death (25–100%).

Patients with specific comorbidities (HIV, dialysis, severe immunosuppression, organ transplant, severe
autoimmune disease and pulmonary hypertension) should be treated in centres able to provide radical
treatment as well as experience in supporting these comorbidities.

Unwanted effects of treatment

For surgery, general anaesthesia, mechanical ventilation and partial collapse of the lung are needed. This
impacts primarily the respiratory system, reducing lung volumes, particularly functional residual capacity,
and causing post-operative complications [10]. Resection causes loss of lung volume, impaired breathing
mechanics and pain, which can increase complications.

Radiotherapy can induce radiation pneumonitis and eventually lung volume loss, and cardiac damage [9,
11–13].

Some systemic treatments such as chemotherapies, e.g. induction chemotherapy, can impair lung function
[14–16]. Immunotherapy can cause pneumonitis [17]. Intercurrent complications such as infections due to
immunosuppression or allergies can further compromise the patient.

Pulmonary function and prognosis

Pre-operatively, forced expiratory volume in 1 s (FEV1) is usually measured. A correlation with pulmonary
complications and mortality is accepted. Pre-operative diffusing capacity of the lung for carbon monoxide
(DLCO) is separately predictive of morbidity and mortality [18, 19]. It is also predictive of toxicity for
chemoradiotherapy [20]. The calculated, estimated post-operative values for FEV1, DLCO and peak oxygen
uptake ( peak V′O2) can give additional information [21, 22].

Exercise tests evaluate overall cardiopulmonary function, and partly also coordination, metabolism and
muscle strength. In particular, peak V′O2 and the slope of minute ventilation to carbon dioxide production
(V′E/V′CO2) during ergo-spirometry are predictive for post-operative complications and mortality [23–27].

Prognostic factors and possible harm by treatments

The natural course of lung cancer is influenced by performance status [28]. It is used as an important
decision factor for treatment. There are also several risk scores published, which are not generally used.

https://doi.org/10.1183/16000617.0195-2023 2
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

The concepts of frailty and nutrition in oncology are also relevant to lung cancer. The prevalence of frailty
in lung cancer is 45%, and frailty increases mortality (hazard ratio 3.01) [29] and therapeutic toxicity (odds
ratio 2.60) [30]. For patients aged >60 years, frailty phenotype assessment can be considered [31].

Malnutrition is prevalent in lung cancer patients and impacts post-operative complications and 1-year
mortality [32]. For patients with underweight or unintentional loss of 10% of their body weight, the
application of the Nutritional Risk Index or Nutritional Risk Score can be considered.

Guidelines for assessing the risk of surgical candidates

Some guidelines have been published for the evaluation for curative therapy. Regarding surgery, especially
the ERS/ESTS and American College of Chest Physicians guidelines have to be mentioned [33, 34]. They
focus on cardiological and pulmonary risk factors and were published several years ago. Meanwhile,
further improvements of peri-operative management (especially enhanced recovery after surgery (ERAS))
and thoracic techniques (video-assisted thoracoscopic surgery (VATS) and robot-assisted thoracic surgery
(RATS)) have occurred [35–37]. Many treatments are now multimodal, including immunotherapy and
advanced radiation techniques.

An Expert Panel of the American Association for Thoracic Surgery Clinical Practice Standards Committee
recently generated a list of important risk factors in the determination of high risk for lobectomy. The most
important factors for high risk were the need for supplemental oxygen because of severe underlying lung
disease, low DLCO, the presence of frailty, and the overall assessment of daily activity and functional
status [38]. A Task Force of the ERS/ESTS is currently updating its guidelines.

Risk reduction by preventive measures and optimisation of general conditions

For surgery, several options for risk minimisation exist: smoking cessation, optimising current treatment of
comorbidities, pre- and post-operative rehabilitation, and optimisation around surgery (ERAS, minimal
invasive thoracic surgery (MITS) and sublobar resection).

Those who quit smoking ∼4 weeks before surgery have a reduced risk of post-surgical complications
[39–41].

In terms of pre- and post-operative rehabilitation, patients who are taught breathing exercises
pre-operatively or who strengthen their respiratory muscles before surgery with a loaded resistive breathing
device can halve their risk of developing post-operative pulmonary complications after major surgery [10].
Pre-operative exercise training improves physical fitness and reduces the risk of post-operative pulmonary
complications while minimising hospital resources utilisation [42]. Exercise training improves exercise
capacity and quadriceps muscle force, and probably quality of life, and decreases dyspnoea following lung
resection for NSCLC [43, 44].

How to choose the right treatment

Multidisciplinary team discussions must consider the patient’s wishes and the individual situation as well
as the available options. The best treatment regarding the tumour may not be the best option for the
patient. For example, in real life, 408 out of 686 (59%) stage III lung cancer patients were considered as
ineligible for concurrent chemoradiation [45]. Experienced centres and interdisciplinary specialist
discussion are important, at least in patients with increased risk. For example, patients with resection for
early-stage NSCLC at facilities with higher use of stereotactic body radiotherapy (SBRT) showed lower
rates of post-operative mortality [46].

Definition of resectability in locally advanced disease

Complete resection is the main aim of a cancer operation. It has been clearly defined for lung cancer
surgery; however, in locally advanced disease, there are peculiarities when mediastinal lymph nodes or
anatomical structures are involved. Complete resection is defined as microscopically tumour-free resection
margins, systematic nodal dissection or lobe-specific systematic nodal dissection, no extracapsular nodal
extension of the tumour and no metastasis in the highest mediastinal node. If any of the aforementioned
criteria are not achieved the resection should be regarded as incomplete. Other criteria that define
incomplete resection are microscopically positive pleural or pericardial effusions [47]. Uncertain resection
is defined as the presence of carcinoma in situ at the bronchial margin or positive pleural lavage cytology
while the resection margins are free and no residual tumour is left [47]. In an oncologically acceptable
operation, ESTS guidelines recommend removal of, at least, three hilar and interlobar nodes and three
mediastinal nodes from three stations in which the subcarinal is always included [48]. Complete resection
and lymph node negativity are proven prognostic factors of long-term survival after resection for locally

https://doi.org/10.1183/16000617.0195-2023 3
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

advanced lung cancer. Thus, pre-resection invasive staging of the hilar and mediastinal lymph nodes is
recommended in these patients. Despite radiologically negative findings, 13–15% lymph node positivity is
found in post-resection specimens [49].

T-based resectability
The 8th edition of the TNM (tumour, node, metastasis) staging system of lung cancer describes locally
advanced disease as a T3 or T4 tumour with intrapulmonary, hilar or mediastinal lymph node involvement
[50]. A T3 tumour is >5 cm but ⩽7 cm in greatest dimension or associated with separate tumour nodule(s)
in the same lobe as the primary tumour or directly invades the chest wall (including the parietal pleura and
superior sulcus tumours), phrenic nerve and parietal pericardium. A T4 tumour is >7 cm in greatest
dimension or associated with separate tumour nodule(s) in a different ipsilateral lobe than that of the
primary tumour or invades the diaphragm, mediastinum, heart, great vessels, trachea, recurrent laryngeal
nerve, oesophagus, vertebral body and carina [50].

Bronchus
There are a few studies suggesting a 1.5–2 cm bronchial resection margin [51, 52]; however, these
suggestions have not been tested in prospective randomised studies and would not be considered strong
evidence. Tumour positivity can be observed in the epithelium, stroma and adventitia of the bronchus [53].
Extramucosal spread has been described as a poor prognostic factor [54]. Safe margins are more frequently
achieved after neoadjuvant treatment [53].

Chest wall
Chest wall invasion is categorised according to the depth of invasion, namely parietal pleura, bony
structures and soft tissues. Depth of invasion is correlated with prognosis, meaning deeper invasion leads
to poorer prognosis [55]. Similarly, a 2 cm clean resection margin is recommended for lung cancers with
chest wall invasion [56]. This not always achievable, especially if the invasion is in the posterior
paravertebral area or thoracic inlet.

Others
Complete en bloc resection with clear margins is associated with favourable prognosis in T4 tumours with
invasion to the carina, vertebra, vena cava, atrium and aorta [57, 58]. However, these are very challenging
cases that require expertise and most of those cases are performed in experienced centres [55, 58–61]. The
results of those series are reported in table 1. Neoadjuvant treatment was shown to improve complete
resection rates and is thus highly recommended in such cases [58]. There is no recommendation for margin
distance; however, a wider margin would lead to a lower local recurrence rate.

N-based resectability
There has been no advantage of complete mediastinal lymph node dissection in early-stage lung cancer if
the sampling of ipsilateral mediastinal lymph nodes was negative for metastasis [62]. It is also evident that
with increasing T stage, the likelihood of mediastinal lymph node metastasis is higher. Thus, a complete
mediastinal lymph node dissection is recommended for accurate staging and complete resection in locally
advanced lung cancer [48].

TABLE 1 Important series in the literature evaluating resection of locally advanced tumours

First author Patients Stage Favourable subgroup 90-day 5-year

(year) [ref.] (n) mortality (%) survival (%)

DODDOLI (2005) [55] 84 T3–4, chest wall, No lymph node involvement, extrathoracic extension NS 29.7
>6 cm
RUSCH (2007) [59] 29 T4, superior Complete pathological response NS 37
sulcus
YILDIZELI (2008) [60] 271 T4 Lymph node negativity, complete resection; subclavian 4# 38.4
artery invasion poor prognostic factor
LI (2019) [61] 1588 T4N0–1 T4 direct tumour invasion 5.7 44.8
TOWE (2021) [58] 1101 T4N0–1 Neoadjuvant treatment (3-fold higher complete NS 54¶
resection rate)
T: tumour; N: node; NS: not stated. #: 30-day mortality; ¶: neoadjuvant treatment group (n=506) survival.

https://doi.org/10.1183/16000617.0195-2023 4
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

N1 disease
Multiple N1 or N1 station ( peripheral/hilar) metastases were associated with poor prognosis compared with
single N1 or N1 station metastasis [63]. Direct invasion to N1 lymph nodes had better survival compared
with hilar lymph node metastasis [64]. There is no proven benefit in terms of locoregional recurrence and
long-term survival by performing a pneumonectomy if the metastatic lymph nodes can be completely
resected with lesser resections and clean margins [63, 64].

N2 disease
Complete resection for N status is defined as nonmetastatic lymph nodes in the highest lymph node station
of the ipsilateral side [48]. This can be interpreted as 2R in the right side and 4L in the left side if a
pre-operative mediastinoscopy or endobronchial ultrasound is not performed to evaluate 2L. Surgical
resection in lung cancer with N2 disease has not been associated with improved survival [65].

However, single-station N2 disease with upper lobe tumours or mediastinal lymph node clearance after
neoadjuvant treatment was associated with significantly longer survival rates [66, 67]. Multiple N2 or
bulky N2 disease is associated with poor survival and a decision should be made in a multidisciplinary
board meeting for these borderline resectable cases [68, 69].

Considerations after neoadjuvant treatment

Neoadjuvant treatment in various forms is intended to achieve responses in the primary tumour. A much
higher rate (almost 30–50%) of major or complete pathological response is observed in locally advanced
lung cancers following neoadjuvant chemoimmunotherapy compared with chemotherapy alone [70].
Handling of the tumour specimen to determine margins is based on a series of recommendations by a
multidisciplinary group [71]. “Tumour bed” is the preferred term to describe the major components,
namely viable tumour, necrosis or stroma which can include inflammation or fibrosis. It is still not clear
how the resection status should be defined if there is a complete response (necrosis or inflammation/
fibrosis) of the tumour at the surgical margin.

Impact of surgical access (open and MIS (VATS and RATS)) on outcome
Surgical resection of lung cancer can be accomplished using various thoracic accesses. The most
commonly used are thoracotomy (also known as the open approach) and MIS access, either by VATS or
RATS. Over the years, numerous variations of these approaches have been developed, utilising different
numbers of ports, various surgical instruments and devices, CO2 insufflation, nonintubated anaesthesia, etc.

Overview of the evidence

Multiple benefits of the VATS approach have been reported [72]. MIS was found to reduce acute and
chronic pain, and thus require a shorter length of hospitalisation [73]. Thoracoscopic lobectomy was
associated with less morbidity and mortality, fewer complications, increased quality of life, and a more
rapid return to function than lobectomy by thoracotomy [74, 75]. In older patients, more independence
after discharge was reported after VATS lobectomy [76]. Thoracoscopic lobectomy was also found to
improve the ability of patients to complete post-operative chemotherapy regimens [77]. Overall costs of
VATS lobectomy were similar to or lower than open lobectomy [78], while RATS was more expensive
and led to longer operating times [79].

Due to their nonrandomised retrospective observational nature, these studies carry a moderate to high bias
prevalence that reduces the generalisability of their findings. A recently published meta-analysis of 19
retrospective trials tried to address this problem [80]. Both MIS approaches (VATS and RATS) were found
superior regarding near-term mortality in early- and advanced-stage lung cancer and elderly patients.
However, benefits were not demonstrated for high-risk patients. Overall survival was similar between open
and MIS approaches in all subgroup comparisons. When comparing RATS with VATS, disease-free
survival was improved when the robotic approach was used, without any significant difference in overall
survival. No statistically significant difference was found regarding overall survival or disease-free survival
when comparing RATS with open procedures [80].

Recently, the results of two large randomised controlled trials (RCTs) studying the impact of VATS access
were also published [81, 82]. Each trial randomised more than 500 patients.

LONG et al. [81] reported that VATS had an advantage in terms of surgery time and bleeding, with similar
short-term complications and outcomes compared with thoracotomy. There were no statistically significant
differences in chest tube duration, length of hospital stay or complications between the two groups.

https://doi.org/10.1183/16000617.0195-2023 5
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

LIM et al. [82] reported that VATS led to a better recovery of physical function at 5 weeks, with no
difference in physical function at 6 and 12 months, compared with thoracotomy, and no difference in
oncological outcomes such as disease-free survival and overall survival. Patients experienced less
in-hospital pain with less analgesic consumption after VATS lobectomy. The benefit was sustained on all
pain-related quality-of-life subscales (including overall, chest and incision pain) documented for up to
1 year. There was no difference in serious adverse events in the hospital, but safety issues, such as
prolonged air leakage and vascular injury, were more common in the VATS group.

A meta-analysis of seven RCTs found that VATS and thoracotomy did not differ in terms of operating
time or early mortality [83]. However, hospital stay was slightly shorter in VATS compared with
thoracotomy. The two approaches also did not differ in terms of bleeding, prolonged air leakage, acute
respiratory failure or arrhythmia. However, the certainty level was low due to a limited number of
complications and significant measurement variations.

Interpretation
There is now a worldwide consensus and a recommendation that MIS techniques should be preferred for
the surgical treatment of lung cancer in patients with no anatomical or surgical contraindications as long as
there is no compromise of the standard oncological and dissection principles of thoracic surgery [84].

Since current evidence indicates that the benefit of MIS is moderate and short lived, a more prudent
recommendation for the use of MIS in lung cancer surgery may be more appropriate, particularly when
utilising MIS in patients with more significant technical challenges and risks of surgical complications,
such as in advanced lung cancer, post-neoadjuvant chemoimmunotherapy [71] and complex pulmonary
resections with bronchovascular reconstructions [85].

There is a significant learning curve associated with VATS lobectomies [86]. When surgeons insufficiently
proficient in MIS are suggested to obsessively utilise this technique to avoid the nonrecommended open
approach, they may unintentionally compromise clinical outcomes due to prolonged surgery time,
increased bleeding [87] or even catastrophic complications [88].

Considering the even longer learning curve associated with anatomical segmental resections [89],
thoracotomy may be still considered in some complex situations for this procedure.

Over the past decades, the open technique has advanced along with MIS. New devices such as
endo-staplers, advanced energy devices, novel surgical instruments, intra-operative magnification and
three-dimensional reconstruction have increased the efficiency of open lung cancer surgery and reduced the
size of the thoracotomy, procedure time and post-operative complications. The utilisation of ERAS has
significantly reduced post-operative morbidity and hospital stay in open lung cancer surgery. At the same
time, the benefit of ERAS in VATS was relatively minor [90]. In a multivariate comparison of predictors
of prolonged hospital stay, the benefit of ERAS in lung cancer surgery was roughly 2-fold compared with
the benefit of VATS [91].

Sublobar versus lobar resection for early-stage NSCLC

An anatomical lobectomy has long been established as the “gold standard” for curative resection of
early-stage lung cancer [92–94]. However, the potential of sublobar resection to better preserve lung
function compared with lobectomy continued to prove alluring to surgeons [95, 96] and clinical experience
accumulated over the last couple of decades has now identified niches where such limited resection may be
an alternative, or even possibly preferable, to lobectomy.

Compromised patients
Because the volume of lung removed is reduced, sublobar resection logically should most benefit
“compromised” patients. A 2016 multicentre study from Japan on patients with clinical stage I lung cancer
who were deemed unfit for lobectomy found that sublobar resection could yield a 3-year overall survival
rate of 79.0% and a 3-year recurrence-free survival rate of 75.9% [97]. Similar results were found in
another Japanese study on patients deemed unfit for lobectomy [98]. Patients with fewer than two “high
risk” factors and undergoing a sublobar resection had a 3-year recurrence-free survival rate of 95%. A
2014 systematic review further found that sublobar resection for patients with clinical stage IA lung cancer
yielded mortality rates of 0–1.4%, 5-year overall survival rates of 40–79% and local recurrence rates of
5.2–5.5% [99]. While these figures are generally inferior to those expected for lobectomy in
noncompromised patients, they are nonetheless acceptable for patients who cannot receive lobectomy.
Moreover, a number of studies have suggested that sublobar resection offered similar morbidity rates as

https://doi.org/10.1183/16000617.0195-2023 6
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

SBRT but possibly better mid- to long-term survival [100, 101]. Such clinical evidence has now led to
sublobar resection (especially segmentectomy) being recognised in major guidelines today as appropriate in
compromised patients with poor pulmonary reserve or other major comorbidities that contraindicate
lobectomy [102, 103].

Intentional sublobar resection

Surveillance Epidemiology End Results (SEER) database results demonstrate significantly worse survival
for small (⩽2 cm) NSCLC patients after intentional sublobar resection than after lobectomy during 1987–
1997 [102]. However, over time, the difference progressively reduced. By 2005–2008, the difference
between sublobar resection and lobectomy was no longer significant [102]. It is probable that this
phenomenon may be the result of two areas of progress: refinement of sublobar surgery and better patient
selection for sublobar resection.

Surgical considerations
Many observational studies over the past two decades have consistently demonstrated that anatomical
segmentectomy offers superior survival to nonanatomical wedge resections when treating stage IA lung
cancer [103, 104]. This may be related to the increased likelihood of segmentectomy achieving wide
resection margins compared with wedge resection. A study from 2007 found that local recurrence after
sublobar resection was significantly more likely if the resection margin was <1 cm [105] and a study from
2013 also found that a wedge resection was significantly more likely to result in a resection margin <1 cm
than a segmentectomy [106]. Nevertheless, the recent CALGB 140503 randomised trial showed equal
5-year survival between sublobar resection and lobectomy for cT1aN0 lung cancer even though the
sublobar arm included 58.8% patients receiving wedge resections [107]. This has generated considerable
discussion over whether wedge resection may eventually prove equivalent to segmentectomy.

The other area where surgical technique may influence the results of sublobar resection is the strategy for
lymph node dissection. Several observational studies have consistently demonstrated that with sublobar
resection for clinical stage I lung cancer, survival is significantly worse in patients where no lymph node
dissection or sampling had been performed [108, 109]. In risk factor analyses for sublobar resection of
lung cancer, lymph node dissection and upstaging have also been shown to be correlated with oncological
outcomes [110, 111]. An elegant study from 2011 showed that sublobar resection (mostly wedge
resections) without lymph node sampling resulted in significantly worse overall and recurrence-free
survival than lobectomy for small (⩽2 cm) NSCLC [112]. However, when sublobar resection was
performed with lymph node sampling, that difference compared with lobectomy was erased. There is
currently broad consensus that nodal dissection should be performed for sublobar resection for lung cancer.
However, much greater controversy exists over what should be done if N1 nodal metastasis is found during
a sublobar resection. One school of thought argues that conversion to a lobectomy is mandatory [113].
However, the opposing school of thought posits that lobectomy is unnecessary, pointing to a number of
studies that have repeatedly shown that lobectomy offers no better survival than segmentectomy should
unexpected N1 nodal metastasis be found [114–116].

Patient selection considerations

The appearance of the target cancer on computed tomography (CT) scanning as a ground-glass opacity
(GGO) or lesion with a consolidation-to-tumour ratio (CTR) <50% generally indicates suitability for
resection by sublobar resection. In risk factor analyses for sublobar resection of lung cancer from Japan,
such CT appearance has been shown to be correlated with oncological outcomes [117, 118]. A systematic
review of 14 cases series from Japan looking at resection of GGOs or lesions with CTR ⩽50% (studies
included 52–100% of all resections by wedge resection or segmentectomy) found that both 5-year overall
and 5-year disease-free survival rates ranged from 93% to 100%, with a local recurrence rate of 0% [119].
It is probable that such GGO or GGO-dominant lesions may represent pre-malignant or less aggressive
forms of adenocarcinoma [120]. The Japanese JCOG0804 multi-institutional confirmatory phase III trial
evaluated the use of sublobar resection for peripheral GGO-dominant lung cancer in 314 patients (82%
wedge resections) and confirmed a 5-year recurrence-free survival rate of 99.7% (95% CI 97.7–100.0%),
with no local relapse [121]. Current guidelines recognise pre-malignant histology and/or CTR <50% as
criteria for choosing to electively perform sublobar resection [93].

The other key criterion in selecting for sublobar resection is a tumour size ⩽2 cm. A meta-analysis of 22
observational studies comparing segmentectomy versus lobectomy for stage I lung cancer in 2013 noted
that the hazard ratios of overall and cancer-specific survival indicated significant benefits of lobectomy for
stage I, stage IA and stage IA with tumours 2–3 cm in size: 1.20 (95% CI 1.04–1.38; p=0.011), 1.24 (95%
CI 1.08–1.42; p=0.002) and 1.41 (95% CI 1.14–1.71; p=0.001), respectively [122]. However, if only

https://doi.org/10.1183/16000617.0195-2023 7
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

tumours ⩽2 cm were considered, segmentectomy provided an effect equivalent to that of lobectomy:

hazard ratio 1.05 (95% CI 0.89–1.24; p=0.550). The most important clinical evidence to date of course
comes from the two major randomised trials comparing sublobar resection versus lobectomy. The Japanese
JCOG0802 trial looked at 1106 patients with peripheral tumours ⩽2 cm and with CTR >50%
(solid-dominant) and found that segmentectomy was noninferior to lobectomy in terms of 5-year overall
survival [36]. The North American CALGB 140503 trial similarly looked at peripheral tumours ⩽2 cm and
found that sublobar resection (58.8% wedge resections) was again noninferior to lobectomy in both 5-year
disease-free and 5-year overall survival rates [107].

Other indications
The rise in interest in sublobar resection coincides with the advent of the era of low-dose CT screening for
lung cancer, which has the potential to reduce lung cancer mortality more than any known treatment
[123–126]. However, current guidelines on how to manage screening-detected lesions tend to recommend
conservative “wait-and-see” approaches for almost all such lesions [93]. This caution arises from a concern
of over-diagnosis (some lesions may not be cancerous), which in turn stems from the perception that
surgical intervention (traditionally lobectomy) is relatively traumatic [127]. Modern sublobar resection
performed via MIS access approaches promises to significantly reduce the morbidity of intervention [128].
There is therefore a school of thought that now suggests a more proactive strategy for intervening and even
resecting screening-detected lesions using sublobar resection, lowering thresholds for considering surgery
[129, 130].

Another increasingly recognised indication for sublobar resection is multifocal lung cancer [131–133]. In
such situations, sublobar resection becomes important to achieve multiple curative resections without
excessive sacrificing of the patient’s lung function [133, 134].

Parenchymal-sparing sleeve resections or pneumonectomy

Sleeve resections of the bronchial tree and/or the pulmonary arterial vasculature are established
parenchymal-sparing resection techniques for centrally located NSCLC with airway or vascular invasion as
well as in tumours directly originating from the airway. Whenever feasible, parenchyma-sparing resection
techniques are preferable over pneumonectomy due to superior peri-operative and long-term outcomes as
well as quality of life. Sleeve resections are feasible from the level of the trachea to the segmental level
with various reconstruction techniques available.

Pre-operative work-up should always include bronchoscopic assessment and consideration of risk factors
for anastomotic healing beyond standard imaging and functional tests [135].

No prospective randomised trial comparing survival after sleeve lobectomy versus pneumonectomy has
been conducted and probably never will be. Thus, approximation of benefit can best be obtained by large,
matched cohorts. A recent propensity score-matched analysis retrospectively compared 665 patients
undergoing sleeve lobectomy with 665 patients undergoing pneumonectomy (9.7% of the sleeve resections
were combined bronchovascular procedures) [136]. Complication rates (3.61% versus 8.72%) as well as
30- and 90-day mortality (0.6% and 1.5% versus 0.9% and 3.91%) were lower in the sleeve group; 5-year
overall survival (61% versus 44.7%) as well as 5-year disease-free survival (56.6% versus 46.2%) were
superior in the sleeve cohort. Another recent study from the same institution compared exclusively 139
bronchovascular sleeve resections with pneumonectomy and found similar results [137].

Functional and oncological outcomes after sleeve lobectomy are comparable to standard lobectomy
[138, 139], even though a higher peri-operative mortality has been described by a single retrospective
analysis which found 5-year survival rates to be comparable again [140].

The ESTS database, one of the largest international thoracic surgical databases, was analysed for patients
undergoing sleeve lobectomy or bilobectomy [141]. 1652 patients were found eligible for analysis. 161
(9.7%) underwent a VATS procedure. Neoadjuvant treatment was given in 24.1% of patients without
increased morbidity or mortality. The overall mortality was low (2.2%) and complication rates were within
the expected range. Bronchial anastomotic complications occurred in 1.8% and in the majority of cases
(79.8%) were managed surgically. The minimally invasive VATS approach was associated with a
decreased post-operative complication rate (odds ratio 0.64, 95% CI 0.42–0.98) in multivariable analysis
and a shorter length of stay (median (interquartile range) 5 (3–8) versus 8 (7–12) days). The conversion
rate, however, was relatively high at 21.1%. Other recent publications confirm the reduced number of
complications after MIS [142] and the noninferiority in survival rate of a VATS approach compared with
open surgery [143].

https://doi.org/10.1183/16000617.0195-2023 8
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

While sleeve lobectomy is a safe procedure, several technical issues can be debated. While some centres
advocated routine coverage of the bronchial anastomosis, in retrospective data of several institutions it
has been shown that neither the number of anastomotic complications nor the peri-operative mortality or
long-term outcome is influenced by wrapping the anastomosis. This is also valid for the subgroup of
patients receiving neoadjuvant chemotherapy or chemoradiotherapy [144]. This also corresponds to the
observations in lung transplantation irrespective of the actual suture technique used [145, 146]. A single
running suture technique is feasible for sleeve resections as well as interrupted stitches on the
cartilaginous portion.

Most of the available single-centre analyses report peri-operative complication rates and mortality in sleeve
resections after neoadjuvant chemotherapy or chemoradiotherapy comparable to primary surgery [147–149].
Adding neoadjuvant immunotherapy neither increases peri-operative morbidity nor mortality [150–152]
and does not seem to impair anastomotic healing. Only limited data are available on the best timing of
sleeve resection after neoadjuvant therapy [153], thus no firm conclusion can be drawn at this stage.

Particularly for low-grade malignancies and tumours directly originating from the central airways, several
advanced parenchymal-sparing resection and reconstruction techniques including neo-carinal formation
have been described; however, these are mainly limited to individual case reports or small case series
[154–158].

Points for clinical practice or future research

• Pre-operative selection of the surgical candidate. The flow of the decision includes: 1) assessment of
respiratory and cardiovascular risk as well as general patient condition and comorbidities; 2) evaluation of
physical activity/exercise capacity and options for improvement; 3) specific therapy options according to
tumour stage, biology and patient situation; 4) assumed oncological outcome (multidisciplinary
discussion); 5) overall evaluation of risks versus benefit (multidisciplinary discussion) and shared decision
making with the patient; and 6) re-evaluation after each therapy step.
• Importance of the surgical access. The ideal surgical access should be individualised to a particular lung
cancer resection. It should provide an optimal balance of safety, speed, cost-efficiency, and short- and
long-term oncological outcomes. Selection should be based on the patient’s characteristics, the surgeon’s
skills, and the whole surgical and hospital environment. The relatively moderate short-term benefits of MIS
over thoracotomy should always be weighed against its potential downsides. Sometimes, this can only be
decided during the procedure. Therefore, any conversion from MIS to thoracotomy should never be seen as
a failure, only performed in case of a vascular injury with severe bleeding. Instead, conversion should be
made as a conscious decision to use thoracotomy to provide the patient with the best outcome of lung
cancer resection.
• Define resectability in locally advanced lung cancer. The following criteria might be used in clinical
practice: 1) ensure a 2 cm margin on the chest wall and safe distance from the tumour on the airway/
bronchus considering peribronchial extension of the tumour; 2) consider tumour-free margins that can be
achieved safely for T4 tumours (no distance recommendations); 3) there is no need for pneumonectomy if
interlobar, hilar lymph nodes are completely removed; 4) perform removal of lymph nodes based on
lymph node staging guideline recommendations; and 5) these cases should always be discussed at
multidisciplinary meetings (in addition, a higher rate of neoadjuvant or peri-operative treatment should be
pursued to achieve higher complete resection rates).
• Lobar versus sublobar resections for early-stage lung cancers. Accumulation of clinical data internationally
has now identified several areas where sublobar resection is justified for the curative treatment of
early-stage lung cancer. In compromised patients who cannot receive lobectomy, sublobar resection offers
acceptable oncological outcomes which may be superior to nonsurgical modalities. In elective situations,
sublobar resection appears appropriate for GGO and GGO-dominant lesions ⩽2 cm in size, preferably with
segmentectomy and lymph node dissection performed. The latest randomised trial data suggest
indications may be extended to even solid and solid-dominant cancers ⩽2 cm in size. The management of
screening-detected lesions and multifocal lung cancer are niches where sublobar resection appears to be
gaining increasing importance.
• Parenchymal-sparing resections for locally advanced lung cancer. Bronchial and bronchovascular sleeve
resections are established routine procedures in the treatment of NSCLC as well as in other tumours
originating from the central airways. Parenchyma-sparing techniques should be used whenever feasible to
achieve a complete resection. Sleeve resections can be safely performed after neoadjuvant therapy including
regimens containing immune checkpoint inhibitors as well as by MIS approaches in selected patients.

https://doi.org/10.1183/16000617.0195-2023 9
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

Provenance: Commissioned article, peer reviewed.

Conflicts of interest: The authors report the following conflicts of interest in the past 36 months. C. Aigner
participated in an advisory board with and received personal consulting fees from AstraZeneca, BMS, MSD, Roche
and Ewimed; and received institutional grants from BMS, Ewimed, PharmaCept, Medtronic and D-A-CH medical
group. H. Batirel participated in an advisory board with and received personal consulting fees from AstraZeneca,
Johnson & Johnson and Medtronic; and is the Secretary General of the ESTS. R.M. Huber participated in an
advisory board with AstraZeneca, Novocure, BMS, Bayer, Roche, Boehringer Ingelheim, Beigene, Sanofi, Janssen
and Merck; and is a co-chair of the ERS/ESTS Task Force on “Fitness for radical therapy in lung cancer” and IASLC
Deputy Chair of the Screening and Early Detection Committee. D.R. Jones has no conflicts to declare. A.D.L. Sihoe
received speaker honoraria from AstraZeneca, Medela, Medtronic and Roche; and is a member of the Board of
Directors of the STS, ASCVTS and Asia Thoracocospic Surgery Education Platform. T. Štupnik received speaker
honoraria from Johnson & Johnson, Roche and MSD; and participated in an advisory board with AstraZeneca and
Johnson & Johnson. A. Brunelli participated in an advisory board with and received personal consulting fees from
AstraZeneca, BMS, MSD, Roche, Johnson & Johnson and Medtronic; and is a co-chair of the ERS/ESTS Task Force
on “Fitness for radical therapy in lung cancer” and member of the Board of Directors of the ESTS and STS.

References
1 Carter BD, Abnet CC, Feskanich D, et al. Smoking and mortality – beyond established causes. N Engl J Med
2015; 372: 631–640.
2 Dy SM, Sharkey P, Herbert R, et al. Comorbid illnesses and health care utilization among Medicare
beneficiaries with lung cancer. Crit Rev Oncol Hematol 2006; 59: 218–225.
3 Hernandez D, Cheng CY, Hernandez-Villafuerte K, et al. Survival and comorbidities in lung cancer patients:
evidence from administrative claims data in Germany. Oncol Res 2022; 30: 173–185.
4 Chida M, Kobayashi S, Karube Y, et al. Incidence of acute exacerbation of interstitial pneumonia in operated
lung cancer: institutional report and review. Ann Thorac Cardiovasc Surg 2012; 18: 314–317.
5 Sekihara K, Aokage K, Oki T, et al. Long-term survival after complete resection of non-small-cell lung cancer
in patients with interstitial lung disease. Interact Cardiovasc Thorac Surg 2018; 26: 638–643.
6 Yamamichi T, Shimada Y, Masuno R, et al. Association between F-18 fluorodeoxyglucose uptake of
noncancerous lung area and acute exacerbation of interstitial pneumonia in patients with lung cancer after
resection. J Thorac Cardiovasc Surg 2020; 159: 1111–1118.
7 Bahig H, Filion E, Vu T, et al. Severe radiation pneumonitis after lung stereotactic ablative radiation therapy
in patients with interstitial lung disease. Pract Radiat Oncol 2016; 6: 367–374.
8 Hagiwara Y, Nakayama Y, Kudo S, et al. Nationwide survey of radiation therapy in Japan for lung cancer
complicated with interstitial lung disease. J Radiat Res 2020; 61: 563–574.
9 Chen H, Senan S, Nossent EJ, et al. Treatment-related toxicity in patients with early-stage non-small cell
lung cancer and coexisting interstitial lung disease: a systematic review. Int J Radiat Oncol Biol Phys 2017;
98: 622–631.
10 Boden I, Denehy L. Respiratory prehabilitation for the prevention of postoperative pulmonary complications
after major surgery. Curr Anesthesiol Rep 2022; 12: 44–58.
11 Banfill K, Giuliani M, Aznar M, et al. Cardiac toxicity of thoracic radiotherapy: existing evidence and future
directions. J Thorac Oncol 2021; 16: 216–227.
12 Wang Q, Liu AH, Fan HJ, et al. The incidences of adverse events in small-cell lung cancer patients after
radiotherapy and immunotherapy treatment: a systematic review and meta-analysis. Eur Rev Med Pharmacol
Sci 2022; 26: 3062–3073.
13 Arroyo-Hernández M, Maldonado F, Lozano-Ruiz F, et al. Radiation-induced lung injury: current evidence.
BMC Pulm Med 2021; 21: 9.
14 Maas KW, van der Lee I, Bolt K, et al. Lung function changes and pulmonary complications in patients with
stage III non-small cell lung cancer treated with gemcitabine/cisplatin as part of combined modality
treatment. Lung Cancer 2003; 41: 345–351.
15 Leo F, Solli P, Spaggiari L, et al. Respiratory function changes after chemotherapy: an additional risk for
postoperative respiratory complications? Ann Thorac Surg 2004; 77: 260–265.
16 Takeda S-i, Funakoshi Y, Kadota Y, et al. Fall in diffusing capacity associated with induction therapy for lung
cancer: a predictor of postoperative complication? Ann Thorac Surg 2006; 82: 232–236.
17 Yin J, Wu Y, Yang X, et al. Checkpoint inhibitor pneumonitis induced by anti-PD-1/PD-L1 therapy in
non-small-cell lung cancer: occurrence and mechanism. Front Immunol 2022; 13: 830631.
18 Ferguson MK, Little L, Rizzo L, et al. Diffusing capacity predicts morbidity and mortality after pulmonary
resection. J Thorac Cardiovasc Surg 1988; 96: 894–900.
19 Bousamra M, Presberg KW, Chammas JH, et al. Early and late morbidity in patients undergoing pulmonary
resection with low diffusion capacity. Ann Thorac Surg 1996; 62: 968–974.

https://doi.org/10.1183/16000617.0195-2023 10
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

20 Videtic GMM, Stitt LW, Ash RB, et al. Impaired diffusion capacity predicts for decreased treatment tolerance
and survival in limited stage small cell lung cancer patients treated with concurrent chemoradiation. Lung
Cancer 2004; 43: 159–166.
21 Ali MK, Mountain CF, Ewer MS, et al. Predicting loss of pulmonary function after pulmonary resection for
bronchogenic carcinoma. Chest 1980; 77: 337–342.
22 Zeiher BG, Gross TJ, Kern JA, et al. Predicting postoperative pulmonary function in patients undergoing
lung resection. Chest 1995; 108: 68–72.
23 Bolliger CT, Jordan P, Solèr M, et al. Pulmonary function and exercise capacity after lung resection. Eur
Respir J 1996; 9: 415–421.
24 Brutsche MH, Spiliopoulos A, Bolliger CT, et al. Exercise capacity and extent of resection as predictors of
surgical risk in lung cancer. Eur Respir J 2000; 15: 828–832.
25 Brunelli A, Belardinelli R, Refai M, et al. Peak oxygen consumption during cardiopulmonary exercise test
improves risk stratification in candidates to major lung resection. Chest 2009; 135: 1260–1267.
26 Benzo R, Kelley GA, Recchi L, et al. Complications of lung resection and exercise capacity: a meta-analysis.
Respir Med 2007; 101: 1790–1797.
27 Brunelli A, Belardinelli R, Pompili C, et al. Minute ventilation-to-carbon dioxide output (V′E/V′CO2) slope is the
strongest predictor of respiratory complications and death after pulmonary resection. Ann Thorac Surg 2012;
93: 1802–1806.
28 Hyde L, Wolf J, McCracken S, et al. Natural course of inoperable lung cancer. Chest 1973; 64: 309–312.
29 Komici K, Bencivenga L, Navani N, et al. Frailty in patients with lung cancer: a systematic review and
meta-analysis. Chest 2022; 162: 485–497.
30 Dai S, Yang M, Song J, et al. Impacts of frailty on prognosis in lung cancer patients: a systematic review and
meta-analysis. Front Med 2021; 8: 715513.
31 Fried LP, Tangen CM, Walston J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci
Med Sci 2001; 56: M146–M156.
32 Lee SC, Lee JG, Lee SH, et al. Prediction of postoperative pulmonary complications using preoperative
controlling nutritional status (CONUT) score in patients with resectable non-small cell lung cancer. Sci Rep
2020; 10: 12385.
33 Brunelli A, Charloux A, Bolliger CT, et al. ERS/ESTS clinical guidelines on fitness for radical therapy in lung
cancer patients (surgery and chemo-radiotherapy). Eur Respir J 2009; 34: 17–41.
34 Brunelli A, Kim AW, Berger KI, et al. Physiologic evaluation of the patient with lung cancer being considered
for resectional surgery: diagnosis and management of lung cancer, 3rd ed: American College of Chest
Physicians evidence-based clinical practice guidelines. Chest 2013; 143; Suppl. 5, e166S–e190S.
35 Batchelor TJP, Rasburn NJ, Abdelnour-Berchtold E, et al. Guidelines for enhanced recovery after lung
surgery: recommendations of the Enhanced Recovery After Surgery (ERAS) Society and the European
Society of Thoracic Surgeons (ESTS). Eur J Cardiothorac Surg 2019; 55: 91–115.
36 Saji H, Okada M, Tsuboi M, et al. Segmentectomy versus lobectomy in small-sized peripheral non-small-cell
lung cancer ( JCOG0802/WJOG4607L): a multicentre, open-label, phase 3, randomised, controlled, non-inferiority
trial. Lancet 2022; 399: 1607–1617.
37 Ma J, Li X, Zhao S, et al. Robot-assisted thoracic surgery versus video-assisted thoracic surgery for lung
lobectomy or segmentectomy in patients with non-small cell lung cancer: a meta-analysis. BMC Cancer
2021; 21: 498.
38 Pennathur A, Brunelli A, Criner GJ, et al. Definition and assessment of high risk in patients considered for
lobectomy for stage I non-small cell lung cancer: the American Association for Thoracic Surgery expert
panel consensus document. J Thorac Cardiovasc Surg 2021; 162: 1605–1618.
39 Yoong SL, Tursan d’Espaignet E, Wiggers J, et al. Tobacco and Postsurgical Outcomes: WHO Tobacco
Knowledge Summaries. 2020. www.who.int/publications/i/item/9789240000360 Date last accessed: 19
January 2024.
40 Caini S, Riccio MD, Vettori V, et al. Quitting smoking at or around diagnosis improves the overall survival of
lung cancer patients: a systematic review and meta-analysis. J Thorac Oncol 2022; 17: 623–636.
41 Young AL, Stefanovska E, Paul C, et al. implementing smoking cessation interventions for tobacco users
within oncology settings: a systematic review. JAMA Oncol 2023; 9: 981–1000.
42 Assouline B, Cools E, Schorer R, et al. Preoperative exercise training to prevent postoperative pulmonary
complications in adults undergoing major surgery. a systematic review and meta-analysis with trial
sequential analysis. Ann Am Thorac Soc 2021; 18: 678–688.
43 Cavalheri V, Burtin C, Formico VR, et al. Exercise training undertaken by people within 12 months of lung
resection for non-small cell lung cancer. Cochrane Database Syst Rev 2019; 6: CD009955.
44 Wang J, Dong Y, Su J, et al. Postoperative exercise training improves the quality of life in patients receiving
pulmonary resection: a systematic review and meta-analysis based on randomized controlled trials. Respir
Med 2022; 192: 106721.

https://doi.org/10.1183/16000617.0195-2023 11
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

45 De Ruysscher D, Botterweck A, Dirx M, et al. Eligibility for concurrent chemotherapy and radiotherapy of
locally advanced lung cancer patients: a prospective, population-based study. Ann Oncol 2009; 20: 98–102.
46 Syed YA, Stokes W, Rupji M, et al. Surgical outcomes for early stage non-small cell lung cancer at facilities
with stereotactic body radiation therapy programs. Chest 2022; 161: 833–844.
47 Rami-Porta R, Wittekind C, Goldstraw P. Complete resection in lung cancer surgery: proposed definition.
Lung Cancer 2005; 49: 25–33.
48 Lardinois D, De Leyn P, Van Schil P, et al. ESTS guidelines for intraoperative lymph node staging in
non-small cell lung cancer. Eur J Cardiothorac Surg 2006; 30: 787–792.
49 El-Osta H, Jani P, Mansour A, et al. Endobronchial ultrasound for nodal staging of patients with
non-small-cell lung cancer with radiologically normal mediastinum. A meta-analysis. Ann Am Thorac Soc
2018; 15: 864–874.
50 Goldstraw P, Chansky K, Crowley J, et al. The IASLC Lung Cancer Staging Project: proposals for revision of
the TNM stage groupings in the forthcoming (eighth) edition of the TNM Classification for lung cancer.
J Thorac Oncol 2016; 11: 39–51.
51 Gunluoglu MZ, Kocaturk CI, Demir A, et al. Bronchial stump recurrence after complete resection of lung
cancer: effect of the distance between the tumor and bronchial resection margin. Thorac Cardiovasc Surg
2018; 66: 156–163.
52 Xiao Z, Zhang M, Liu Z, et al. Distance between tumor and bronchial resection margin is an independent
predictor of recurrence-free survival and overall survival in primary endobronchial neoplasm. J Cancer Res
Clin Oncol 2023; 149: 11171–11180.
53 Sato H, Toyooka S, Soh J, et al. Advantage of induction chemoradiotherapy for lung cancer in securing
cancer-free bronchial margin. Ann Thorac Surg 2017; 104: 971–978.
54 Kaiser LR, Fleshner P, Keller S, et al. Significance of extramucosal residual tumor at the bronchial resection
margin. Ann Thorac Surg 1989; 47: 265–269.
55 Doddoli C, D’Journo B, Le Pimpec-Barthes F, et al. Lung cancer invading the chest wall: a plea for en-bloc
resection but the need for new treatment strategies. Ann Thorac Surg 2005; 80: 2032–2040.
56 Wang L, Yan X, Zhao J, et al. Expert consensus on resection of chest wall tumors and chest wall
reconstruction. Transl Lung Cancer Res 2021; 10: 4057–4083.
57 Fadel E, Missenard G, Court C, et al. Long-term outcomes of en bloc resection of non-small cell lung cancer
invading the thoracic inlet and spine. Ann Thorac Surg 2011; 92: 1024–1030.
58 Towe CW, Worrell SG, Bachman K, et al. Neoadjuvant treatment is associated with superior outcomes in T4
lung cancers with local extension. Ann Thorac Surg 2021; 111: 448–455.
59 Rusch VW, Giroux DJ, Kraut MJ, et al. Induction chemoradiation and surgical resection for superior sulcus
non-small-cell lung carcinomas: long-term results of Southwest Oncology Group Trial 9416 (Intergroup Trial
0160). J Clin Oncol 2007; 25: 313–318.
60 Yildizeli B, Dartevelle PG, Fadel E, et al. Results of primary surgery with T4 non-small cell lung cancer during
a 25-year period in a single center: the benefit is worth the risk. Ann Thorac Surg 2008; 86: 1065–1075.
61 Li Q, Zhang P, Wang Y, et al. T4 extension alone is more predictive of better survival than a tumour size
>7 cm for resected T4N0–1M0 non-small-cell lung cancer. Eur J Cardiothorac Surg 2019; 55: 682–690.
62 Darling GE, Allen MS, Decker PA, et al. Randomized trial of mediastinal lymph node sampling versus
complete lymphadenectomy during pulmonary resection in the patient with N0 or N1 (less than hilar)
non-small cell carcinoma: results of the American College of Surgery Oncology Group Z0030 trial. J Thorac
Cardiovasc Surg 2011; 141: 662–670.
63 Demir A, Turna A, Kocaturk C, et al. Prognostic significance of surgical-pathologic N1 lymph node
involvement in non-small cell lung cancer. Ann Thorac Surg 2009; 87: 1014–1022.
64 Marra A, Hillejan L, Zaboura G, et al. Pathologic N1 non-small cell lung cancer: correlation between pattern
of lymphatic spread and prognosis. J Thorac Cardiovasc Surg 2003; 125: 543–553.
65 Albain KS, Swann RS, Rusch VW, et al. Radiotherapy plus chemotherapy with or without surgical resection
for stage III non-small-cell lung cancer: a phase III randomised controlled trial. Lancet 2009; 374: 379–386.
66 Inoue M, Sawabata N, Takeda S, et al. Results of surgical intervention for p-stage IIIA (N2) non-small cell
lung cancer: acceptable prognosis predicted by complete resection in patients with single N2 disease with
primary tumor in the upper lobe. J Thorac Cardiovasc Surg 2004; 127: 1100–1106.
67 Betticher DC, Hsu Schmitz SF, Tötsch M, et al. Mediastinal lymph node clearance after docetaxel-cisplatin
neoadjuvant chemotherapy is prognostic of survival in patients with stage IIIA pN2 non-small-cell lung
cancer: a multicenter phase II trial. J Clin Oncol 2003; 21: 1752–1759.
68 Kang CH, Ra YJ, Kim YT, et al. The impact of multiple metastatic nodal stations on survival in patients with
resectable N1 and N2 nonsmall-cell lung cancer. Ann Thorac Surg 2008; 86: 1092–1097.
69 Sakuraba M, Takahashi N, Oh S, et al. Long-term survival after complete mediastinal lymph node resection
and lobectomy in patients with bulky N2 non-small cell lung cancer. Ann Thorac Cardiovasc Surg 2011; 17:
124–129.

https://doi.org/10.1183/16000617.0195-2023 12
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

70 Travis WD, Dacic S, Wistuba I, et al. IASLC multidisciplinary recommendations for pathologic assessment of
lung cancer resection specimens after neoadjuvant therapy. J Thorac Oncol 2020; 15: 709–740.
71 Forde PM, Spicer J, Lu S, et al. Neoadjuvant nivolumab plus chemotherapy in resectable lung cancer. N Engl
J Med 2022; 386: 1973–1985.
72 Whitson BA, Groth SS, Duval SJ, et al. 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 2008; 86: 2008–2016.
73 Scott WJ, Allen MS, Darling G, et al. Video-assisted thoracic surgery versus open lobectomy for lung cancer:
a secondary analysis of data from the American College of Surgeons Oncology Group Z0030 randomized
clinical trial. J Thorac Cardiovasc Surg 2010; 139: 976–981.
74 Paul S, Altorki NK, Sheng S, et al. Thoracoscopic lobectomy is associated with lower morbidity than open
lobectomy: a propensity-matched analysis from the STS database. J Thorac Cardiovasc Surg 2010; 139:
366–378.
75 Cao C, Manganas C, Ang SC, et al. Video-assisted thoracic surgery versus open thoracotomy for non-small
cell lung cancer: a meta-analysis of propensity score-matched patients. Interact Cardiovasc Thorac Surg
2013; 16: 244–249.
76 Demmy TL, Plante AJ, Nwogu CE, et al. Discharge independence with minimally invasive lobectomy. Am
J Surg 2004; 188: 698–702.
77 Nicastri DG, Wisnivesky JP, Litle VR, et al. Thoracoscopic lobectomy: report on safety, discharge
independence, pain, and chemotherapy tolerance. J Thorac Cardiovasc Surg 2008; 135: 642–647.
78 Fiorelli A, Forte S, Caronia FP, et al. Is video-assisted thoracoscopic lobectomy associated with higher overall
costs compared with open surgery? Results of best evidence topic analysis. Thorac Cancer 2021; 12:
567–579.
79 Nakamura H. Systematic review of published studies on safety and efficacy of thoracoscopic and
robot-assisted lobectomy for lung cancer. Ann Thorac Cardiovasc Surg 2014; 20: 93–98.
80 Manerikar A, Querrey M, Cerier E, et al. Comparative effectiveness of surgical approaches for lung cancer.
J Surg Res 2021; 263: 274–284.
81 Long H, Tan Q, Luo Q, et al. Thoracoscopic surgery versus thoracotomy for lung cancer: short-term
outcomes of a randomized trial. Ann Thorac Surg 2018; 105: 386–392.
82 Lim E, Batchelor TJP, Dunning J, et al. Video-assisted thoracoscopic or open lobectomy in early-stage lung
cancer. NEJM Evidence 2022; 1: EVIDoa2100016.
83 Kim D, Woo W, Shin JI, et al. The uncomfortable truth: open thoracotomy versus minimally invasive surgery
in lung cancer: a systematic review and meta-analysis. Cancers 2023; 15: 2630.
84 Ettinger DS, Wood DE, Aisner DL, et al. NCCN Guidelines Insights: Non-Small Cell Lung Cancer, Version
2.2023: featured updates to the NCCN Guidelines. J Natl Compr Cancer Netw 2023; 21: 340–350.
85 Xie D, Zhong Y, Deng J, et al. Comparison of uniportal video-assisted thoracoscopic versus thoracotomy
bronchial sleeve lobectomy with pulmonary arterioplasty for centrally located non-small-cell lung cancer.
Eur J Cardiothorac Surg 2021; 59: 978–986.
86 Zhao H, Bu L, Yang F, et al. Video-assisted thoracoscopic surgery lobectomy for lung cancer: the learning
curve. World J Surg 2010; 34: 2368–2372.
87 Dexter E, Attwood K, Demmy T, et al. Does operative duration of lobectomy for early lung cancer increase
perioperative morbidity? Ann Thorac Surg 2022; 114: 941–947.
88 Flores RM, Ihekweazu U, Dycoco J, et al. Video-assisted thoracoscopic surgery (VATS) lobectomy:
catastrophic intraoperative complications. J Thorac Cardiovasc Surg 2011; 142: 1412–1417.
89 Hamada A, Oizumi H, Kato H, et al. Learning curve for port-access thoracoscopic anatomic lung
segmentectomy. J Thorac Cardiovasc Surg 2018; 156: 1995–2003.
90 Van Haren RM, Mehran RJ, Mena GE, et al. Enhanced recovery decreases pulmonary and cardiac
complications after thoracotomy for lung cancer. Ann Thorac Surg 2018; 106: 272–279.
91 Rogers LJ, Bleetman D, Messenger DE, et al. The impact of enhanced recovery after surgery (ERAS) protocol
compliance on morbidity from resection for primary lung cancer. J Thorac Cardiovasc Surg 2018; 155:
1843–1852.
92 Howington JA, Blum MG, Chang AC, et al. Treatment of stage I and II non-small cell lung cancer: diagnosis
and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical
practice guidelines. Chest 2013; 143: Suppl. 5, e278S–e313S.
93 National Comprehensive Cancer Network. Clinical Practice Guidelines in Oncology. Non-Small Cell Lung
Cancer Version 3.2023. 2023. www.nccn.org/professionals/physician_gls/pdf/nscl.pdf Date last accessed: 17
September 2023.
94 Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell
lung cancer. Lung Cancer Study Group. Ann Thorac Surg 1995; 60: 615–622.
95 Keenan RJ, Landreneau RJ, Maley RH Jr, et al. Segmental resection spares pulmonary function in patients
with stage I lung cancer. Ann Thorac Surg 2004; 78: 228–233.

https://doi.org/10.1183/16000617.0195-2023 13
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

96 Harada H, Okada M, Sakamoto T, et al. Functional advantage after radical segmentectomy versus lobectomy
for lung cancer. Ann Thorac Surg 2005; 80: 2041–2045.
97 Takahashi N, Sawabata N, Kawamura M, et al. Optimal sublobar resection for c-stage I non-small cell lung
cancer: significance of margin distance to tumor size ratio and margin cytology (supplementary analysis of
KLSG-0801): complete republication. Gen Thorac Cardiovasc Surg 2019; 67: 690–696.
98 Hattori A, Takamochi K, Matsunaga T, et al. Oncological outcomes of sublobar resection for clinical-stage IA
high-risk non-small cell lung cancer patients with a radiologically solid appearance on computed
tomography. Gen Thorac Cardiovasc Surg 2016; 64: 18–24.
99 De Ruysscher D, Nakagawa K, Asamura H. Surgical and nonsurgical approaches to small-size nonsmall cell
lung cancer. Eur Respir J 2014; 44: 483–494.
100 Mahmood S, Bilal H, Faivre-Finn C, et al. Is stereotactic ablative radiotherapy equivalent to sublobar
resection in high-risk surgical patients with stage I non-small-cell lung cancer? Interact Cardiovasc Thorac
Surg 2013; 17: 845–853.
101 Crabtree T, Puri V, Timmerman R, et al. Treatment of stage I lung cancer in high-risk and inoperable
patients: comparison of prospective clinical trials using stereotactic body radiotherapy (RTOG 0236),
sublobar resection (ACOSOG Z4032), and radiofrequency ablation (ACOSOG Z4033). J Thorac Cardiovasc Surg
2013; 145: 692–699.
102 Yendamuri S, Sharma R, Demmy M, et al. Temporal trends in outcomes following sublobar and lobar
resections for small (⩽2 cm) non-small cell lung cancers – a Surveillance Epidemiology End Results
database analysis. J Surg Res 2013; 183: 27–32.
103 Sienel W, Dango S, Kirschbaum A, et al. Sublobar resections in stage IA non-small cell lung cancer:
segmentectomies result in significantly better cancer-related survival than wedge resections. Eur J
Cardiothorac Surg 2008; 33: 728–734.
104 Li G, Xie S, Hu F, et al. Segmentectomy or wedge resection in stage IA lung squamous cell carcinoma and
adenocarcinoma? J Cancer 2021; 12: 1708–1714.
105 El-Sherif A, Fernando HC, Santos R, et al. Margin and local recurrence after sublobar resection of non-small
cell lung cancer. Ann Surg Oncol 2007; 14: 2400–2405.
106 Kent M, Landreneau R, Mandrekar S, et al. Segmentectomy versus wedge resection for non-small cell lung
cancer in high-risk operable patients. Ann Thorac Surg 2013; 96: 1747–1754.
107 Altorki N, Wang X, Kozono D, et al. Lobar or sublobar resection for peripheral stage IA non-small-cell lung
cancer. N Engl J Med 2023; 388: 489–498.
108 Stiles BM, Kamel MK, Nasar A, et al. The importance of lymph node dissection accompanying wedge
resection for clinical stage IA lung cancer. Eur J Cardiothorac Surg 2017; 51: 511–517.
109 Speicher PJ, Gu L, Gulack BC, et al. Sublobar resection for clinical stage IA non-small-cell lung cancer in the
United States. Clin Lung Cancer 2016; 17: 47–55.
110 Zhou H, Tapias LF, Gaissert HA, et al. Lymph node assessment and impact on survival in video-assisted
thoracoscopic lobectomy or segmentectomy. Ann Thorac Surg 2015; 100: 910–916.
111 Moon Y, Lee KY, Park JK. Prognosis after sublobar resection of small-sized non-small cell lung cancer with
visceral pleural or lymphovascular invasion. World J Surg 2017; 41: 2769–2777.
112 Wolf AS, Richards WG, Jaklitsch MT, et al. Lobectomy versus sublobar resection for small (2 cm or less)
non-small cell lung cancers. Ann Thorac Surg 2011; 92: 1819–1823.
113 Gossot D, Mariolo AV, Lefevre M, et al. Strategies of lymph node dissection during sublobar resection for
early-stage lung cancer. Front Surg 2021; 8: 725005.
114 Nomori H, Mori T, Izumi Y, et al. Is completion lobectomy merited for unanticipated nodal metastases after
radical segmentectomy for cT1 N0 M0/pN1-2 non-small cell lung cancer? J Thorac Cardiovasc Surg 2012;
143: 820–824.
115 Lutfi W, Schuchert MJ, Dhupar R, et al. Node-positive segmentectomy for non-small-cell lung cancer: risk
factors and outcomes. Clin Lung Cancer 2019; 20: e463–e469.
116 Razi SS, Nguyen D, Villamizar N. Lobectomy does not confer survival advantage over segmentectomy for
non-small cell lung cancer with unsuspected nodal disease. J Thorac Cardiovasc Surg 2020; 159: 2469–2483.
117 Koike T, Koike T, Yamato Y, et al. Prognostic predictors in non-small cell lung cancer patients undergoing
intentional segmentectomy. Ann Thorac Surg 2012; 93: 1788–1794.
118 Sakairi Y, Yoshino I, Yoshida S, et al. Pattern of metastasis outside tumor-bearing segments in primary lung
cancer: rationale for segmentectomy. Ann Thorac Surg 2014; 97: 1694–1700.
119 Detterbeck FC, Homer RJ. Approach to the ground-glass nodule. Clin Chest Med 2011; 32: 799–810.
120 Gao JW, Rizzo S, Ma LH, et al. Pulmonary ground-glass opacity: computed tomography features,
histopathology and molecular pathology. Transl Lung Cancer Res 2017; 6: 68–75.
121 Suzuki K, Watanabe S, Wakabayashi M, et al. A nonrandomized confirmatory phase III study of sublobar
surgical resection for peripheral ground glass opacity dominant lung cancer defined with thoracic
thin-section computed tomography ( JCOG0804/WJOG4507L). J Clin Oncol 2017; 35: 8561.

https://doi.org/10.1183/16000617.0195-2023 14
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

122 Bao F, Ye P, Yang Y, et al. Segmentectomy or lobectomy for early stage lung cancer: a meta-analysis. Eur J
Cardiothorac Surg 2014; 46: 1–7.
123 The National Lung Screening Trial Research Team. Reduced lung-cancer mortality with low-dose computed
tomographic screening. N Engl J Med 2011; 365: 395–409.
124 de Koning HJ, van der Aalst CM, de Jong PA, et al. Reduced lung-cancer mortality with volume CT screening
in a randomized trial. N Engl J Med 2020; 382: 503–551.
125 Yang PC. PS01.02 National lung cancer screening program in Taiwan: the TALENT study. J Thorac Oncol
2021; 16: S58.
126 Yu SWY, Leung CS, Tsz CH, et al. Does low-dose computed tomography screening improve lung
cancer-related outcomes? A systematic review. Video-assist Thorac Surg 2020; 5: 7.
127 US Preventive Services Task Force. Screening for lung cancer: US Preventive Services Task Force
recommendation statement. JAMA 2021; 325: 962–970.
128 Sihoe ADL. Video-assisted thoracoscopic surgery as the gold standard for lung cancer surgery. Respirology
2020; 25: Suppl. 2, 49–60.
129 Sihoe ADL. Should sublobar resection be offered for screening-detected lung nodules? Transl Lung Cancer
Res 2021; 10: 2418–2426.
130 Zheng D, Chen H. Lung cancer screening in China: early-stage lung cancer and minimally invasive surgery
3.0. J Thorac Dis 2018; 10: Suppl. 14, S1677–S1679.
131 Kozower BD, Larner JM, Detterbeck FC, et al. Special treatment issues in non-small cell lung cancer:
diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based
clinical practice guidelines. Chest 2013; 143: Suppl. 5, e369S–e399S.
132 Zhao L, Liu C, Xie G, et al. Multiple primary lung cancers: a new challenge in the era of precision medicine.
Cancer Manag Res 2020; 12: 10361–10374.
133 Suzuki K. Whack-a-mole strategy for multifocal ground glass opacities of the lung. J Thorac Dis 2017; 9:
Suppl. 3, S201–S207.
134 Sihoe ADL, Van Schil P. Non-small cell lung cancer: when to offer sublobar resection. Lung Cancer 2014; 86:
115–120.
135 Collaud S, Alnajdawi Y, Stork T, et al. Preoperative chest computed tomography evaluation for predicting
intraoperative lung resection strongly depends on interpreters experience. Lung Cancer 2021; 154: 23–28.
136 Chen J, Soultanis KM, Sun F, et al. Outcomes of sleeve lobectomy versus pneumonectomy: a propensity
score-matched study. J Thorac Cardiovasc Surg 2021; 162: 1619–1628.
137 Yang M, Zhong Y, Deng J, et al. Comparison of bronchial sleeve lobectomy with pulmonary arterioplasty
versus pneumonectomy. Ann Thorac Surg 2022; 113: 934–941.
138 D’Andrilli A, Maurizi G, Andreetti C, et al. Sleeve lobectomy versus standard lobectomy for lung cancer:
functional and oncologic evaluation. Ann Thorac Surg 2016; 101: 1936–1942.
139 Inci I, Benker M, Çitak N, et al. Complex sleeve lobectomy has the same surgical outcome when compared
with conventional lobectomy in patients with lung cancer. Eur J Cardiothorac Surg 2020; 57: 860–866.
140 Zalepugas D, Koryllos A, Stoelben E, et al. Sleeve lobectomy versus lobectomy for primary treatment of
non-small-cell lung cancer: a single-center retrospective analysis. J Surg Oncol 2021; 123: 553–559.
141 Gonzalez M, Chriqui LE, Décaluwé H, et al. Sleeve lobectomy in patients with non-small-cell lung cancer:
a report from the European Society of Thoracic Surgery database 2021. Eur J Cardiothorac Surg 2022; 62:
ezac502.
142 Li X, Li Q, Yang F, et al. Neoadjuvant therapy does not increase postoperative morbidity of sleeve lobectomy
in locally advanced non-small cell lung cancer. J Thorac Cardiovasc Surg 2023; 166: 1234–1244.
143 Nitsche LJ, Jordan S, Demmy T, et al. Analyzing the impact of minimally invasive surgical approaches on
post-operative outcomes of pneumonectomy and sleeve lobectomy patients. J Thorac Dis 2023; 15:
2497–2504.
144 Storelli E, Tutic M, Kestenholz P, et al. Sleeve resections with unprotected bronchial anastomoses are safe
even after neoadjuvant therapy. Eur J Cardiothorac Surg 2012; 42: 77–81.
145 Aigner C, Jaksch P, Seebacher G, et al. Single running suture – the new standard technique for bronchial
anastomoses in lung transplantation. Eur J Cardiothorac Surg 2003; 23: 488–493.
146 FitzSullivan E, Gries CJ, Phelan P, et al. Reduction in airway complications after lung transplantation with
novel anastomotic technique. Ann Thorac Surg 2011; 92: 309–315.
147 Veronesi G, Solli PG, Leo F, et al. Low morbidity of bronchoplastic procedures after chemotherapy for lung
cancer. Lung Cancer 2002; 36: 91–97.
148 Milman S, Kim AW, Warren WH, et al. The incidence of perioperative anastomotic complications after sleeve
lobectomy is not increased after neoadjuvant chemoradiotherapy. Ann Thorac Surg 2009; 88: 945–950.
149 Gómez-Caro A, Boada M, Reguart N, et al. Sleeve lobectomy after induction chemoradiotherapy. Eur J
Cardiothorac Surg 2012; 41: 1052–1058.

https://doi.org/10.1183/16000617.0195-2023 15
EUROPEAN RESPIRATORY REVIEW POTENTIALLY OPERABLE LUNG CANCER | C. AIGNER ET AL.

150 Romero Román A, Campo-Cañaveral de la Cruz JL, Macía I, et al. Outcomes of surgical resection after
neoadjuvant chemoimmunotherapy in locally advanced stage IIIA non-small-cell lung cancer. Eur J
Cardiothorac Surg 2021; 60: 81–88.
151 Rusch VW, Nicholas A, Patterson GA, et al. Surgical results of the Lung Cancer Mutation Consortium 3 trial:
a phase II multicenter single-arm study to investigate the efficacy and safety of atezolizumab as
neoadjuvant therapy in patients with stages IB-select IIIB resectable non-small cell lung cancer. J Thorac
Cardiovasc Surg 2023; 165: 828–839.
152 Stefani D, Plönes T, Viehof J, et al. Lung cancer surgery after neoadjuvant immunotherapy. Cancers 2021;
13: 4033.
153 Koryllos A, Lopez-Pastorini A, Zalepugas D, et al. Optimal timing of surgery for bronchial sleeve resection
after neoadjuvant chemoradiotherapy. J Surg Oncol 2020; 122: 328–335.
154 Chen L, Campisi A, Wang Z, et al. Left secondary carinal resection and reconstruction for low-grade
bronchial malignancies. JTCVS Tech 2021; 8: 196–201.
155 Stamatis G, Fechner S, Rocha M, et al. Resection of the tracheobronchial bifurcation with complete
preservation of lung parenchyma. Ann Thorac Surg 2017; 104: 1741–1747.
156 Lang G, Taghavi S, Aigner C, et al. Extracorporeal membrane oxygenation support for resection of locally
advanced thoracic tumors. Ann Thorac Surg 2011; 92: 264–270.
157 Date N, Yutaka Y, Date H. Successful lung-sparing carinal reconstruction after induction chemoradiotherapy
for carinal cancer via median sternotomy: reefing bronchial membrane technique. JTCVS Tech 2022; 17:
170–173.
158 Gonzalez-Rivas D, Essa RA, Motas N, et al. Uniportal robotic-assisted thoracic surgery lung-sparing carinal
sleeve resection and reconstruction. Ann Cardiothorac Surg 2023; 12: 130–132.

https://doi.org/10.1183/16000617.0195-2023 16