Reimplantation of the upper lobe bronchus after lower sleeve lobectomy or bilobectomy: long-term results

Reimplantation of the upper lobe bronchus after lower sleeve lobectomy or bilobectomy: long-term... Abstract OBJECTIVES The advantages of a bronchial sleeve resection are well established. A clear majority of reported cases are of upper lobe sleeve resection. Reimplantation of the upper lobe bronchus after a lower sleeve lobectomy or bilobectomy (the so-called Y-sleeve resection) is infrequent. Related technical peculiarities are the main issues. We present our experience and results in this setting. METHODS Between 1989 and 2015, we performed 28 Y-sleeve resections of the left lower lobe (n = 18) or right middle and lower lobes (n = 10). The lung-sparing reconstructive operation was performed for non-small-cell lung cancer in 23 cases, for bronchial carcinoid tumour in 4 cases and for a cystic adenoid carcinoma in 1 case. Anastomotic reconstruction was performed by interrupted 4-0 absorbable sutures (monofilament material). RESULTS All the resections were complete (R0). Postoperative mortality was 3.6%. The rate of major complications was 10.7% (1 myocardial infarction, 1 anastomotic stenosis requiring dilatation and 1 anastomotic fistula). Among the 23 patients with non-small-cell lung cancer (18 men and 5 women; mean age 58 ± 12 years), 8 were Stage I, 9 were Stage II and 6 were Stage IIIa. At a mean follow-up of 46 months, the recurrence rate was 32%. There were 2 loco-regional recurrences. No endobronchial or perianastomotic recurrence occurred. The 3- and 5-year overall and disease-free survival rates of patients with non-small-cell lung cancer were 76.3% and 55.1% and 68.7% and 62.9%, respectively. CONCLUSIONS A Y-sleeve resection with reimplantation of the upper load bronchus is a technically feasible and oncologically adequate operation. Lung cancer, Lobectomy, Sleeve resection INTRODUCTION Sleeve lobectomy is a reliable surgical option to avoid pneumonectomy for patients with centrally located lung cancer who cannot be radically treated by a standard lobectomy [1–4]. The advantages of a bronchial sleeve resection are well established [5–8]. This parenchymal sparing operation is usually considered when the tumour infiltrates the origin of a lobar bronchus. However, a majority of the reported cases are an upper lobe sleeve resection with reimplantation of the lower lobe bronchus or the bronchus intermedius [9]. Reimplantation of the upper lobe bronchus (ULB) after a lower sleeve lobectomy or a bilobectomy (the Y-sleeve resection) [10] is infrequent. On the left side, a Y bronchial resection is required when the tumour arises at the origin of the lower lobe bronchus. On the right side, the traditional indication for a Y-sleeve resection (here also called a sleeve bilobectomy) is a tumour that infiltrates the origin of the bronchus intermedius, thus requiring the sacrifice of both the medium and lower lobes with no possibility of performing a standard lower bilobectomy. Technical difficulties related to reconstruction include size discrepancy, proximity to the pulmonary artery, poor exposure of the mediastinal side of the anastomosis and its proximity to the segmental division of the upper lobe. These main technical issues, the relatively infrequent occurrence and the potential risk of complications still limit the use of this reconstructive operation among thoracic surgeons. To the best of our knowledge, a series including only patients undergoing ULB anastomotic reimplantation after bronchial Y-sleeve reconstruction for lung cancer has never been reported. In this study, we present our experience and results in this setting. MATERIALS AND METHODS Between 1989 and 2015, 28 patients underwent a Y-sleeve reconstruction of the left lower lobe (n = 18) or right middle and lower lobes (n = 10). A lung-sparing reconstructive operation was performed for non-small-cell lung cancer (NSCLC) in 23 cases, for bronchial carcinoid tumour in 4 cases and for a cystic adenoid carcinoma in 1 case. During the same study period, 149 major lung resections (pneumonectomy) and 312 sleeve lobectomies were performed for centrally located tumours. The prevalence of Y-sleeve resections among the total number of sleeve lobectomies was 9%. This study was approved by the local ethics committee and was conducted in accordance with the Declaration of Helsinki. All the patients provided written informed consent for the surgical intervention and for the inclusion of their personal data in a scientific database. Preoperative non-invasive evaluation and staging included contrast-enhanced thoracic and abdominal computed tomography (CT), brain CT or magnetic resonance imaging and bone scintigraphy. Since 2004, 18F-fluorodeoxyglucose whole-body positron emission tomography (PET) was performed in cases in whom the presence of metastases was in doubt. A preoperative clinical workup to assess the operability of the patients included respiratory function tests and a blood gas analysis. In case of doubt on functional resectability, perfusion lung scintigraphy was associated. A preoperative invasive study that included flexible bronchoscopy was performed in all patients to assess the involvement of the bronchial tree and to obtain a diagnosis. Mediastinoscopy was performed in the presence of enlarged peritracheal or subcarinal lymph nodes (long-axis diameter >1.5 cm) noted on a CT scan. All patients with histologically or cytologically proven metastatic mediastinal lymph nodes received induction chemotherapy. Since 2004, after chemotherapy and before surgery, mediastinal restaging was performed by PET-CT scans (by contrast-enhanced CT scans before 2004). Transbronchial needle aspiration was performed only in selected cases if persistent N2 disease was suspected after neoadjuvant treatment. All the patients were clinical N0–1, some of whom after induction therapy. Systematic hilar and mediastinal lymphadenectomy was performed on all patients. Postoperative flexible bronchoscopy was performed at 1, 3 and 6 months and once a year for the following 5 years. Follow-up examinations were scheduled every 6 months for the first 5 years. Since 2004, postoperative non-invasive follow-up examinations were performed with contrast-enhanced whole-body CT scans, bone scintigraphy and 18F fluorodeoxyglucose-PET. All of the patients who survived were available for follow-up for the first 5 years. The last follow-up examination was February 2017. Surgical technique The surgical approach was a lateral muscle-sparing thoracotomy in all the patients. On the right side, a sleeve bilobectomy was performed for an endoluminal lesion in the bronchus intermedius that extended upwards, proximal to the upper lobe orifice. The right mainstem bronchus was divided at this level just proximal to the right upper lobe take-off and the right ULB was divided at its origin. The ULB was anastomosed to the mainstem bronchus after removal of the middle and lower lobes (the Y-sleeve resection) (Fig. 1A). Frozen sections were always analysed to validate the radicality of the resection. If the margins were positive, pneumonectomy was considered. Figure 1: View largeDownload slide Drawings illustrating the so-called Y-sleeve resection; the ULB is reimplanted to the mainstem bronchus. (A) Right lower sleeve bilobectomy. (B) Left lower sleeve lobectomy. ULB: upper lobe bronchus. Figure 1: View largeDownload slide Drawings illustrating the so-called Y-sleeve resection; the ULB is reimplanted to the mainstem bronchus. (A) Right lower sleeve bilobectomy. (B) Left lower sleeve lobectomy. ULB: upper lobe bronchus. Figure 2: View largeDownload slide Intraoperative picture showing left mainstem bronchus, upper lobe bronchus and lower lobe bronchus after Y resection. Figure 2: View largeDownload slide Intraoperative picture showing left mainstem bronchus, upper lobe bronchus and lower lobe bronchus after Y resection. Anastomotic reconstruction was performed by interrupted 4-0 absorbable sutures (monofilament material). According to our technique [11], the first stitch was placed in an ‘outside-to-in’ fashion at the junction of the cartilaginous and membranous bronchi. These few initial sutures were immediately tied to confer improved stability to this point of the anastomosis. Additional sutures were placed at 2-mm intervals to complete the first half of the cartilaginous anastomosis. When the midpoint of the cartilaginous bronchus was reached, the anastomosis was completed on the opposite side of the bronchial circumference in a similar fashion. Sutures were then tied beginning from either end of the cartilaginous portion and working towards the middle. Placing and tying the sutures in this order allowed us to compensate for even large-calibre discrepancies. This technique prevented torsion of the bronchial axis and gently stretched and dilated the circumference of the distal bronchus. Due to the reorientation of the ULB after removal of the middle and lower lobes, we used exceptional care to avoid twisting the bronchus at the level of the anastomosis. The ULB was reimplanted directly on the carina in 3 patients. For resection of lesions infiltrating the left lower lobe orifice with extension into the mainstem bronchus but sparing the upper lobe orifice, a lower lobectomy with sleeve resection of the left main bronchus was performed. After completion of the bronchial dissection, an umbilical tape was passed around the left mainstem and left upper lobe bronchi. The left ULB was divided at its origin. Next, the mainstem bronchus was divided proximally to the bifurcation and well beyond the extent of the tumour (Figs 1B and 2). Once the margins were confirmed to be negative by analysis of the frozen sections, anastomotic reconstruction was performed according to the previously illustrated technique (Fig. 3A and B). However, on the left side, when there was no calibre discrepancy, due to the narrowing and poor exposure of the mediastinal side of the anastomosis, a partial continuous running suture was sometimes used only in this portion. The lingular bronchus might arise proximally to the section line, and care was taken when dividing the ULB to ensure that it remained intact. An intercostal muscle flap to protect the bronchial anastomosis was routinely used; the technique for intercostal muscle flap harvesting and transposition was described previously [12]. Low-dose steroids was administered in all the patients in the postoperative period with the aim of antioedema effect, thus reducing secretion retention and atelectasis and minimizing the risk of granuloma formation and dehiscence. Figure 3: View largeDownload slide Intraoperative picture showing the anastomotic reimplantation of the upper lobe bronchus after the left lower sleeve lobectomy. (A) Separate stitches are passed but still untied. (B) Completed anastomosis. Figure 3: View largeDownload slide Intraoperative picture showing the anastomotic reimplantation of the upper lobe bronchus after the left lower sleeve lobectomy. (A) Separate stitches are passed but still untied. (B) Completed anastomosis. Statistical analysis Data were collected and stored in an Excel database (Microsoft Corp., Redmond, WA, USA). All statistical analyses were performed using IBM-SPSS Statistics (version 21.0.0.0). Quantitative variables are expressed as mean ± standard deviation. Overall and disease-free survival rates were estimated with the Kaplan–Meier method only for those patients with NSCLC. RESULTS Nineteen patients were men and 9 were women. The mean age was 56.3 ± 12.2 years (range 34–79). Significant comorbidities were present in 6 patients (cardiac ischaemic disease in 2, diabetes in 3, chronic obstructive pulmonary disease in 3, renal insufficiency in 1 and chronic atrial fibrillation in 1). The mean predicted preoperative forced expiratory volume in 1 s was 90.2 ± 14.8% (range 61.9–115.8%). Preoperative mediastinal node involvement was assessed by mediastinoscopy in 2 patients who consequently underwent induction chemotherapy. Both patients with histologically proven clinical N2 presented no evidence of mediastinal disease after chemotherapy at the clinical re-evaluation performed by a PET-CT scan. The histological diagnosis was squamous cell carcinoma in 15 patients, adenocarcinoma in 6 patients, mixed and large-cell carcinoma in 1 patient, bronchial carcinoid tumour in 4 patients and cystic adenoid carcinoma in 1 patient. Of the 23 patients with NSCLC (18 men and 5 women; mean age 58 ± 12 years), 8 were Stage pI (p = pathological), 9 were Stage pII and 6 were Stage pIIIa. All Stage pIIIa were pN2. All the resections were complete (R0). One elderly patient who had severe diabetes and was unfit for pneumonectomy died of sepsis following a bronchopleural fistula occurring in the anastomotic site (3.6%). The overall postoperative morbidity rate was 25% (n = 7). The major complications rate was 10.7% (n = 3). Postoperative major complications included myocardial infarction (1 patient), anastomotic fistula evolving into pleural empyema (1 patient) and anastomotic stenosis that was successfully treated by laser (1 patient). Other complications included atrial fibrillation (2 patients), parenchymal air leak (1 patient) and retention of secretions (1 patient). Nine patients underwent adjuvant chemotherapy. Complete long-term patency of the reconstructed airway was documented in all the patients by fibre-optic bronchoscopy. According to the NSCLC histological analysis, at a mean follow-up of 46 months, range (2–117), the recurrence rate was 32%. There were 2 loco-regional recurrences (9%; 1 mediastinal and 1 at the hilum of the contralateral lung). No endobronchial or perianastomotic recurrence occurred. The 3- and 5-year overall and disease-free survival rates of patients who had NSCLC were 76.3% and 55.1% and 68.7% and 62.9% (Figs 4 and 5), respectively. Figure 4: View largeDownload slide Overall survival curve (Kaplan–Meier). Figure 4: View largeDownload slide Overall survival curve (Kaplan–Meier). Figure 5: View largeDownload slide Disease-free survival curve (Kaplan–Meier). Figure 5: View largeDownload slide Disease-free survival curve (Kaplan–Meier). The 3- and 5-year overall survival rates of patients with NSCLC according to the stage was 100% and 83.3% for Stage I, 77.8% and 55.6% for Stage II and 31.3% and 0% for Stage III, respectively (Fig. 6). The 3- and 5-year disease-free survival rates were both 85.7% for Stage I, 85.7 and 71.4 for Stage II and both 0% for Stage III (Fig. 7). Figure 6: View largeDownload slide Overall survival curve according to the pathological stage (Kaplan–Meier). Figure 6: View largeDownload slide Overall survival curve according to the pathological stage (Kaplan–Meier). Figure 7: View largeDownload slide Disease-free survival curve according to the pathological stage (Kaplan–Meier). Figure 7: View largeDownload slide Disease-free survival curve according to the pathological stage (Kaplan–Meier). DISCUSSION Sleeve lobectomy has proven to be a safe and oncologically reliable operation for patients with lung cancer; our and other authors’ decades-long experiences prove this statement, even after the introduction of neoadjuvant chemotherapy [13–16]. The principles of the Y-sleeve resection with the anastomotic reimplantation of the ULB are very similar to those of other sleeve lobectomies, except for some technical and perioperative management peculiarities [17]. When considering the technical aspects, the size discrepancy of the bronchial stumps, the proximity to the pulmonary artery, the poor exposure of the mediastinal side of the anastomosis and its proximity to the upper lobe segmental division are the main issues. Size discrepancy is more frequent on the right side. It can be efficiently addressed by an interrupted-sutures anastomosis [18]. Sometimes, on the left side, when the calibre discrepancy is negligible, the current author’s choice is a partial continuous suture on the mediastinal portion of the anastomosis due to the narrow and difficult exposure on this side. The proximity of the pulmonary artery to the site of the airway reconstruction can add additional difficulties for the surgeon. For these reasons, the technique must be performed carefully. We and other authors [19] prefer the open approach rather than a video-assisted [20–22] procedure, thus allowing a more precise placement of the stitches keeping the sutures well organized. Endobronchial tumoural infiltration requiring such a reconstructive technique, in particular on the right side, occurs infrequently. In fact, a tumour arising at the origin of the left lower lobe bronchus or a tumour involving the middle and lower lobes up to the origin of bronchus intermedius usually infiltrates the fissures and the pulmonary artery branches for the upper lobe. This occurrence has to be managed by pneumonectomy when possible. Some authors have described a lower sleeve lobectomy extended to the lingular segment when infiltrated [23–25]. In our experience, the 90° angle between the mainstem bronchus and the ULB does not represent a technical issue for a tension-free realignment of the 2 bronchial stumps and anastomotic reconstruction. The most common complication after the Y-sleeve procedure is the retention of secretions [19]. Therefore, in the postoperative period, repeated bronchoscopies are needed as well as, in our experience, the administration of low doses of steroids. We believe that the antioedema effect of steroids is advantageous because it can reduce secretion retention and atelectasis, and it can minimize the risk of granuloma formation and dehiscence. Aerosolized steroids are also a part of our preoperative procedure when sleeve lobectomy can be predicted beforehand. In our experience, patients treated with steroids show a reduced need for bronchoscopy in the postoperative period. Kinking of the left superior pulmonary vein has been reported as a theoretical complication [26], but we did not observe such a complication. The largest and most important published experiences on sleeve lobectomies report small numbers of Y sleeve with reimplantation of ULB [27]. However, almost none of these articles report either the precise number of patients undergoing such bronchial reconstructive procedures or the results from this subset of patients [9, 28, 29]. Park et al. [3] reported a series of 38 patients undergoing left lower or right middle and lower sleeve lobectomy out of a total of 157 patients having sleeve lobectomies performed over a decade with no information about the short- or long-term results of this subgroup of patients. To the best of our knowledge, this is the first series that includes patients only undergoing a left lower sleeve lobectomy or a right sleeve bilobectomy. The data from our retrospective series are in line with those of other studies including sleeve lobectomy that show functional advantages and comparable oncological outcome with respect to PN [1, 7, 8, 29, 30]. The oncological reliability of this surgical procedure is supported by the absence of local recurrence at the level of bronchial reconstruction observed in our long-term results. Given the limitation due to the small number of patients included in this series, the poor long-term survival in Stage III patients could have been negatively influenced by the high rate of cases of squamous cell carcinomas with a reduced response to adjuvant therapy. Moreover, all Stage pIIIa cases were pN2 patients, thus confirming the consolidated literature data showing N2 as the main factor affecting survival after bronchovascular reconstruction [27, 29, 30]. The present experience demonstrates that these airway reconstructions can be made without the increased jeopardy of complications. It is even more true when morbidity and mortality rates are compared with those of series including patients who undergo pneumonectomy [1]. This study has some limitations: First, the study included a small number of patients collected over a long period. The second limitation of this study is its retrospective nature. The main strength is the homogeneous series of interventions performed by the same surgical group with unmodified indications, technique and management over time. The strengths of the study are the complete long-term follow-up and the regular distribution of patients over the study period. CONCLUSION In conclusion, left lower and right middle and lower SR with reimplantation of the ULB seem to be technically feasible and oncologically adequate over the long term when the patient is carefully selected and the operation is meticulously performed. ACKNOWLEDGEMENTS We thank Marta Silvi for data management and editorial work. Conflict of interest: none declared. REFERENCES 1 Shi W, Zhang W, Sun H, Shao Y. Sleeve lobectomy versus pneumonectomy for non-small cell lung cancer: a meta-analysis. World J Surg Oncol  2012; 10: 265. Google Scholar CrossRef Search ADS PubMed  2 Ferguson MK, Lehman AG. Sleeve lobectomy or pneumonectomy: optimal management strategy using decision analysis techniques. Ann Thorac Surg  2003; 76: 1782– 8. Google Scholar CrossRef Search ADS PubMed  3 Park JS, Yang HC, Kim HK, Kim K, Shim YM, Choi YS. Sleeve lobectomy as an alternative procedure to pneumonectomy for non-small cell lung cancer. J Thorac Oncol  2010; 5: 517– 20. Google Scholar CrossRef Search ADS PubMed  4 Gómez-Caro A, Garcia S, Reguart N, Cladellas E, Arguis P, Sanchez M et al.   Determining the appropriate sleeve lobectomy versus pneumonectomy ratio in central non-small cell lung cancer patients: an audit of an aggressive policy of pneumonectomy avoidance. Eur J Cardiothorac Surg  2011; 39: 352– 9. 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Google Scholar PubMed  8 Melloul E, Egger B, Krueger T, Cheng C, Mithieux F, Ruffieux C et al.   Mortality, complications and loss of pulmonary function after pneumonectomy vs. sleeve lobectomy in patients younger and older than 70 years. Interact CardioVasc Thorac Surg  2008; 7: 986– 9. Google Scholar CrossRef Search ADS PubMed  9 Merritt RE, Mathisen DJ, Wain JC, Gaissert HA, Donahue D, Lanuti M et al.   Long-term results of sleeve lobectomy in the management of non-small cell lung carcinoma and low-grade neoplasms. Ann Thorac Surg  2009; 88: 1574– 81; discussion 1581–2. Google Scholar CrossRef Search ADS PubMed  10 Ciccone AM, Venuta F, Rendina EA. Bronchoplastic procedures. In: Kaiser LR, Kron IL, Spray TL (eds). Mastery of Cardiothoracic Surgery, 2nd edn . Philadelphia: Lippincott Williams & Wilkins, 2007, 64– 70. 11 Maurizi G, D’Andrilli A, Venuta F, Rendina EA. Bronchial and arterial sleeve resection for centrally-located lung cancers. J Thorac Dis  2016; 8: S872– 81. 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Google Scholar CrossRef Search ADS PubMed  16 Milman S, Kim AW, Warren WH, Liptay MJ, Miller C, Basu S et al.   The incidence of perioperative anastomotic complications after sleeve lobectomy is not increased after neoadjuvant chemoradiotherapy. Ann Thorac Surg  2009; 88: 945– 50; discussion 950–1. Google Scholar CrossRef Search ADS PubMed  17 Maurizi G, D’Andrilli A, Venuta F, Rendina EA. Reconstruction of the bronchus and pulmonary artery. J Thorac Dis  2016; 8: S168– 80. Google Scholar CrossRef Search ADS PubMed  18 Rendina EA, Venuta F, Ciriaco P, Ricci C. Bronchovascular sleeve resection. Technique, perioperative management, prevention and treatment of complications. J Thorac Cardiovasc Surg  1993; 106: 73– 9. Google Scholar PubMed  19 Mathisen DJ. Right lower and middle lobe sleeve lobectomy. In: Mathisen DJ, Morse CR (eds). Thoracic Surgery: Lung Resections, Bronchoplasty . Philadelphia: Wolters Kluwer, 2015, 375– 81. 20 Gonzalez-Rivas D, Delgado M, Fieira E, Pato O. Left lower sleeve lobectomy by uniportal ideo-assisted thoracoscopic approach. Interact CardioVasc Thorac Surg  2014; 18: 237– 9. Google Scholar CrossRef Search ADS PubMed  21 Zhang X, Peng GL, Liang LX, He JX. Right, middle, and lower bronchial sleeve lobectomy by video-assisted thoracic surgery. J Thorac Dis  2013; 5: S277– 9. Google Scholar PubMed  22 Fan JQ, Yao J, Chang ZB, Wang Q, Zhao BQ. Left lower sleeve lobectomy and systematic lymph node dissection by complete video-assisted thoracic surgery. J Thorac Dis  2014; 6: 1826– 30. Google Scholar PubMed  23 Okada M, Tsubota N, Yoshimura M, Miyamoto Y, Matsuoka H, Satake S et al.   Extended sleeve lobectomy for lung cancer (the avoidance of pneumonectomy). J Thorac Cardiovasc Surg  1999; 118: 710– 14. Google Scholar CrossRef Search ADS PubMed  24 Berthet JP, Paradela M, Jimenez MJ, Molins L, Gómez-Caro A. Extended sleeve lobectomy: one more step toward avoiding pneumonectomy in centrally located lung cancer. Ann Thorac Surg  2013; 96: 1988– 97. Google Scholar CrossRef Search ADS PubMed  25 Pan X, Chen Y, Shi J, Zhao H, Chen H. Robotic assisted extended sleeve lobectomy after neoadjuvant chemotherapy. Ann Thorac Surg  2015; 100: e129– 31. Google Scholar CrossRef Search ADS PubMed  26 Ugalde PA, Gregorie J, Zhinguang Y, Boultifat R, Deslauriers J. Left lower lobe sleeve resection. In: Mathisen DJ, Morse CR (eds). Thoracic Surgery: Lung Resections, Bronchoplasty . Philadelphia: Wolters Kluwer, 2015, 391– 4. 27 Yildizeli B, Fadel E, Mussot S, Fabre D, Chataigner O, Dartevelle PG. Morbidity, mortality, and long-term survival after sleeve lobectomy for non-small cell lung cancer. Eur J Cardiothorac Surg  2007; 31: 95– 102. Google Scholar CrossRef Search ADS PubMed  28 Pagès PB, Mordant P, Renaud S, Brouchet L, Thomas PA, Dahan M et al.  ; Epithor Project (French Society of Thoracic and Cardiovascular Surgery). Sleeve lobectomy may provide better outcomes than pneumonectomy for non-small cell lung cancer. A decade in a nationwide study. J Thorac Cardiovasc Surg  2017; 153: 184– 95.e3. Google Scholar CrossRef Search ADS PubMed  29 Deslauriers J, Grégoire J, Jacques LF, Piraux M, Guojin L, Lacasse Y. Sleeve lobectomy versus pneumonectomy for lung cancer: a comparative analysis of survival and sites or recurrences. Ann Thorac Surg  2004; 77: 1152– 6; discussion 1156. Google Scholar CrossRef Search ADS PubMed  30 Ludwig C, Stoelben E, Olschewski M, Hasse J. Comparison of morbidity, 30-day mortality, and long-term survival after pneumonectomy and sleeve lobectomy for non-small cell lung carcinoma. Ann Thorac Surg  2005; 79: 968– 73. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2018. Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved. 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Reimplantation of the upper lobe bronchus after lower sleeve lobectomy or bilobectomy: long-term results

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Abstract

Abstract OBJECTIVES The advantages of a bronchial sleeve resection are well established. A clear majority of reported cases are of upper lobe sleeve resection. Reimplantation of the upper lobe bronchus after a lower sleeve lobectomy or bilobectomy (the so-called Y-sleeve resection) is infrequent. Related technical peculiarities are the main issues. We present our experience and results in this setting. METHODS Between 1989 and 2015, we performed 28 Y-sleeve resections of the left lower lobe (n = 18) or right middle and lower lobes (n = 10). The lung-sparing reconstructive operation was performed for non-small-cell lung cancer in 23 cases, for bronchial carcinoid tumour in 4 cases and for a cystic adenoid carcinoma in 1 case. Anastomotic reconstruction was performed by interrupted 4-0 absorbable sutures (monofilament material). RESULTS All the resections were complete (R0). Postoperative mortality was 3.6%. The rate of major complications was 10.7% (1 myocardial infarction, 1 anastomotic stenosis requiring dilatation and 1 anastomotic fistula). Among the 23 patients with non-small-cell lung cancer (18 men and 5 women; mean age 58 ± 12 years), 8 were Stage I, 9 were Stage II and 6 were Stage IIIa. At a mean follow-up of 46 months, the recurrence rate was 32%. There were 2 loco-regional recurrences. No endobronchial or perianastomotic recurrence occurred. The 3- and 5-year overall and disease-free survival rates of patients with non-small-cell lung cancer were 76.3% and 55.1% and 68.7% and 62.9%, respectively. CONCLUSIONS A Y-sleeve resection with reimplantation of the upper load bronchus is a technically feasible and oncologically adequate operation. Lung cancer, Lobectomy, Sleeve resection INTRODUCTION Sleeve lobectomy is a reliable surgical option to avoid pneumonectomy for patients with centrally located lung cancer who cannot be radically treated by a standard lobectomy [1–4]. The advantages of a bronchial sleeve resection are well established [5–8]. This parenchymal sparing operation is usually considered when the tumour infiltrates the origin of a lobar bronchus. However, a majority of the reported cases are an upper lobe sleeve resection with reimplantation of the lower lobe bronchus or the bronchus intermedius [9]. Reimplantation of the upper lobe bronchus (ULB) after a lower sleeve lobectomy or a bilobectomy (the Y-sleeve resection) [10] is infrequent. On the left side, a Y bronchial resection is required when the tumour arises at the origin of the lower lobe bronchus. On the right side, the traditional indication for a Y-sleeve resection (here also called a sleeve bilobectomy) is a tumour that infiltrates the origin of the bronchus intermedius, thus requiring the sacrifice of both the medium and lower lobes with no possibility of performing a standard lower bilobectomy. Technical difficulties related to reconstruction include size discrepancy, proximity to the pulmonary artery, poor exposure of the mediastinal side of the anastomosis and its proximity to the segmental division of the upper lobe. These main technical issues, the relatively infrequent occurrence and the potential risk of complications still limit the use of this reconstructive operation among thoracic surgeons. To the best of our knowledge, a series including only patients undergoing ULB anastomotic reimplantation after bronchial Y-sleeve reconstruction for lung cancer has never been reported. In this study, we present our experience and results in this setting. MATERIALS AND METHODS Between 1989 and 2015, 28 patients underwent a Y-sleeve reconstruction of the left lower lobe (n = 18) or right middle and lower lobes (n = 10). A lung-sparing reconstructive operation was performed for non-small-cell lung cancer (NSCLC) in 23 cases, for bronchial carcinoid tumour in 4 cases and for a cystic adenoid carcinoma in 1 case. During the same study period, 149 major lung resections (pneumonectomy) and 312 sleeve lobectomies were performed for centrally located tumours. The prevalence of Y-sleeve resections among the total number of sleeve lobectomies was 9%. This study was approved by the local ethics committee and was conducted in accordance with the Declaration of Helsinki. All the patients provided written informed consent for the surgical intervention and for the inclusion of their personal data in a scientific database. Preoperative non-invasive evaluation and staging included contrast-enhanced thoracic and abdominal computed tomography (CT), brain CT or magnetic resonance imaging and bone scintigraphy. Since 2004, 18F-fluorodeoxyglucose whole-body positron emission tomography (PET) was performed in cases in whom the presence of metastases was in doubt. A preoperative clinical workup to assess the operability of the patients included respiratory function tests and a blood gas analysis. In case of doubt on functional resectability, perfusion lung scintigraphy was associated. A preoperative invasive study that included flexible bronchoscopy was performed in all patients to assess the involvement of the bronchial tree and to obtain a diagnosis. Mediastinoscopy was performed in the presence of enlarged peritracheal or subcarinal lymph nodes (long-axis diameter >1.5 cm) noted on a CT scan. All patients with histologically or cytologically proven metastatic mediastinal lymph nodes received induction chemotherapy. Since 2004, after chemotherapy and before surgery, mediastinal restaging was performed by PET-CT scans (by contrast-enhanced CT scans before 2004). Transbronchial needle aspiration was performed only in selected cases if persistent N2 disease was suspected after neoadjuvant treatment. All the patients were clinical N0–1, some of whom after induction therapy. Systematic hilar and mediastinal lymphadenectomy was performed on all patients. Postoperative flexible bronchoscopy was performed at 1, 3 and 6 months and once a year for the following 5 years. Follow-up examinations were scheduled every 6 months for the first 5 years. Since 2004, postoperative non-invasive follow-up examinations were performed with contrast-enhanced whole-body CT scans, bone scintigraphy and 18F fluorodeoxyglucose-PET. All of the patients who survived were available for follow-up for the first 5 years. The last follow-up examination was February 2017. Surgical technique The surgical approach was a lateral muscle-sparing thoracotomy in all the patients. On the right side, a sleeve bilobectomy was performed for an endoluminal lesion in the bronchus intermedius that extended upwards, proximal to the upper lobe orifice. The right mainstem bronchus was divided at this level just proximal to the right upper lobe take-off and the right ULB was divided at its origin. The ULB was anastomosed to the mainstem bronchus after removal of the middle and lower lobes (the Y-sleeve resection) (Fig. 1A). Frozen sections were always analysed to validate the radicality of the resection. If the margins were positive, pneumonectomy was considered. Figure 1: View largeDownload slide Drawings illustrating the so-called Y-sleeve resection; the ULB is reimplanted to the mainstem bronchus. (A) Right lower sleeve bilobectomy. (B) Left lower sleeve lobectomy. ULB: upper lobe bronchus. Figure 1: View largeDownload slide Drawings illustrating the so-called Y-sleeve resection; the ULB is reimplanted to the mainstem bronchus. (A) Right lower sleeve bilobectomy. (B) Left lower sleeve lobectomy. ULB: upper lobe bronchus. Figure 2: View largeDownload slide Intraoperative picture showing left mainstem bronchus, upper lobe bronchus and lower lobe bronchus after Y resection. Figure 2: View largeDownload slide Intraoperative picture showing left mainstem bronchus, upper lobe bronchus and lower lobe bronchus after Y resection. Anastomotic reconstruction was performed by interrupted 4-0 absorbable sutures (monofilament material). According to our technique [11], the first stitch was placed in an ‘outside-to-in’ fashion at the junction of the cartilaginous and membranous bronchi. These few initial sutures were immediately tied to confer improved stability to this point of the anastomosis. Additional sutures were placed at 2-mm intervals to complete the first half of the cartilaginous anastomosis. When the midpoint of the cartilaginous bronchus was reached, the anastomosis was completed on the opposite side of the bronchial circumference in a similar fashion. Sutures were then tied beginning from either end of the cartilaginous portion and working towards the middle. Placing and tying the sutures in this order allowed us to compensate for even large-calibre discrepancies. This technique prevented torsion of the bronchial axis and gently stretched and dilated the circumference of the distal bronchus. Due to the reorientation of the ULB after removal of the middle and lower lobes, we used exceptional care to avoid twisting the bronchus at the level of the anastomosis. The ULB was reimplanted directly on the carina in 3 patients. For resection of lesions infiltrating the left lower lobe orifice with extension into the mainstem bronchus but sparing the upper lobe orifice, a lower lobectomy with sleeve resection of the left main bronchus was performed. After completion of the bronchial dissection, an umbilical tape was passed around the left mainstem and left upper lobe bronchi. The left ULB was divided at its origin. Next, the mainstem bronchus was divided proximally to the bifurcation and well beyond the extent of the tumour (Figs 1B and 2). Once the margins were confirmed to be negative by analysis of the frozen sections, anastomotic reconstruction was performed according to the previously illustrated technique (Fig. 3A and B). However, on the left side, when there was no calibre discrepancy, due to the narrowing and poor exposure of the mediastinal side of the anastomosis, a partial continuous running suture was sometimes used only in this portion. The lingular bronchus might arise proximally to the section line, and care was taken when dividing the ULB to ensure that it remained intact. An intercostal muscle flap to protect the bronchial anastomosis was routinely used; the technique for intercostal muscle flap harvesting and transposition was described previously [12]. Low-dose steroids was administered in all the patients in the postoperative period with the aim of antioedema effect, thus reducing secretion retention and atelectasis and minimizing the risk of granuloma formation and dehiscence. Figure 3: View largeDownload slide Intraoperative picture showing the anastomotic reimplantation of the upper lobe bronchus after the left lower sleeve lobectomy. (A) Separate stitches are passed but still untied. (B) Completed anastomosis. Figure 3: View largeDownload slide Intraoperative picture showing the anastomotic reimplantation of the upper lobe bronchus after the left lower sleeve lobectomy. (A) Separate stitches are passed but still untied. (B) Completed anastomosis. Statistical analysis Data were collected and stored in an Excel database (Microsoft Corp., Redmond, WA, USA). All statistical analyses were performed using IBM-SPSS Statistics (version 21.0.0.0). Quantitative variables are expressed as mean ± standard deviation. Overall and disease-free survival rates were estimated with the Kaplan–Meier method only for those patients with NSCLC. RESULTS Nineteen patients were men and 9 were women. The mean age was 56.3 ± 12.2 years (range 34–79). Significant comorbidities were present in 6 patients (cardiac ischaemic disease in 2, diabetes in 3, chronic obstructive pulmonary disease in 3, renal insufficiency in 1 and chronic atrial fibrillation in 1). The mean predicted preoperative forced expiratory volume in 1 s was 90.2 ± 14.8% (range 61.9–115.8%). Preoperative mediastinal node involvement was assessed by mediastinoscopy in 2 patients who consequently underwent induction chemotherapy. Both patients with histologically proven clinical N2 presented no evidence of mediastinal disease after chemotherapy at the clinical re-evaluation performed by a PET-CT scan. The histological diagnosis was squamous cell carcinoma in 15 patients, adenocarcinoma in 6 patients, mixed and large-cell carcinoma in 1 patient, bronchial carcinoid tumour in 4 patients and cystic adenoid carcinoma in 1 patient. Of the 23 patients with NSCLC (18 men and 5 women; mean age 58 ± 12 years), 8 were Stage pI (p = pathological), 9 were Stage pII and 6 were Stage pIIIa. All Stage pIIIa were pN2. All the resections were complete (R0). One elderly patient who had severe diabetes and was unfit for pneumonectomy died of sepsis following a bronchopleural fistula occurring in the anastomotic site (3.6%). The overall postoperative morbidity rate was 25% (n = 7). The major complications rate was 10.7% (n = 3). Postoperative major complications included myocardial infarction (1 patient), anastomotic fistula evolving into pleural empyema (1 patient) and anastomotic stenosis that was successfully treated by laser (1 patient). Other complications included atrial fibrillation (2 patients), parenchymal air leak (1 patient) and retention of secretions (1 patient). Nine patients underwent adjuvant chemotherapy. Complete long-term patency of the reconstructed airway was documented in all the patients by fibre-optic bronchoscopy. According to the NSCLC histological analysis, at a mean follow-up of 46 months, range (2–117), the recurrence rate was 32%. There were 2 loco-regional recurrences (9%; 1 mediastinal and 1 at the hilum of the contralateral lung). No endobronchial or perianastomotic recurrence occurred. The 3- and 5-year overall and disease-free survival rates of patients who had NSCLC were 76.3% and 55.1% and 68.7% and 62.9% (Figs 4 and 5), respectively. Figure 4: View largeDownload slide Overall survival curve (Kaplan–Meier). Figure 4: View largeDownload slide Overall survival curve (Kaplan–Meier). Figure 5: View largeDownload slide Disease-free survival curve (Kaplan–Meier). Figure 5: View largeDownload slide Disease-free survival curve (Kaplan–Meier). The 3- and 5-year overall survival rates of patients with NSCLC according to the stage was 100% and 83.3% for Stage I, 77.8% and 55.6% for Stage II and 31.3% and 0% for Stage III, respectively (Fig. 6). The 3- and 5-year disease-free survival rates were both 85.7% for Stage I, 85.7 and 71.4 for Stage II and both 0% for Stage III (Fig. 7). Figure 6: View largeDownload slide Overall survival curve according to the pathological stage (Kaplan–Meier). Figure 6: View largeDownload slide Overall survival curve according to the pathological stage (Kaplan–Meier). Figure 7: View largeDownload slide Disease-free survival curve according to the pathological stage (Kaplan–Meier). Figure 7: View largeDownload slide Disease-free survival curve according to the pathological stage (Kaplan–Meier). DISCUSSION Sleeve lobectomy has proven to be a safe and oncologically reliable operation for patients with lung cancer; our and other authors’ decades-long experiences prove this statement, even after the introduction of neoadjuvant chemotherapy [13–16]. The principles of the Y-sleeve resection with the anastomotic reimplantation of the ULB are very similar to those of other sleeve lobectomies, except for some technical and perioperative management peculiarities [17]. When considering the technical aspects, the size discrepancy of the bronchial stumps, the proximity to the pulmonary artery, the poor exposure of the mediastinal side of the anastomosis and its proximity to the upper lobe segmental division are the main issues. Size discrepancy is more frequent on the right side. It can be efficiently addressed by an interrupted-sutures anastomosis [18]. Sometimes, on the left side, when the calibre discrepancy is negligible, the current author’s choice is a partial continuous suture on the mediastinal portion of the anastomosis due to the narrow and difficult exposure on this side. The proximity of the pulmonary artery to the site of the airway reconstruction can add additional difficulties for the surgeon. For these reasons, the technique must be performed carefully. We and other authors [19] prefer the open approach rather than a video-assisted [20–22] procedure, thus allowing a more precise placement of the stitches keeping the sutures well organized. Endobronchial tumoural infiltration requiring such a reconstructive technique, in particular on the right side, occurs infrequently. In fact, a tumour arising at the origin of the left lower lobe bronchus or a tumour involving the middle and lower lobes up to the origin of bronchus intermedius usually infiltrates the fissures and the pulmonary artery branches for the upper lobe. This occurrence has to be managed by pneumonectomy when possible. Some authors have described a lower sleeve lobectomy extended to the lingular segment when infiltrated [23–25]. In our experience, the 90° angle between the mainstem bronchus and the ULB does not represent a technical issue for a tension-free realignment of the 2 bronchial stumps and anastomotic reconstruction. The most common complication after the Y-sleeve procedure is the retention of secretions [19]. Therefore, in the postoperative period, repeated bronchoscopies are needed as well as, in our experience, the administration of low doses of steroids. We believe that the antioedema effect of steroids is advantageous because it can reduce secretion retention and atelectasis, and it can minimize the risk of granuloma formation and dehiscence. Aerosolized steroids are also a part of our preoperative procedure when sleeve lobectomy can be predicted beforehand. In our experience, patients treated with steroids show a reduced need for bronchoscopy in the postoperative period. Kinking of the left superior pulmonary vein has been reported as a theoretical complication [26], but we did not observe such a complication. The largest and most important published experiences on sleeve lobectomies report small numbers of Y sleeve with reimplantation of ULB [27]. However, almost none of these articles report either the precise number of patients undergoing such bronchial reconstructive procedures or the results from this subset of patients [9, 28, 29]. Park et al. [3] reported a series of 38 patients undergoing left lower or right middle and lower sleeve lobectomy out of a total of 157 patients having sleeve lobectomies performed over a decade with no information about the short- or long-term results of this subgroup of patients. To the best of our knowledge, this is the first series that includes patients only undergoing a left lower sleeve lobectomy or a right sleeve bilobectomy. The data from our retrospective series are in line with those of other studies including sleeve lobectomy that show functional advantages and comparable oncological outcome with respect to PN [1, 7, 8, 29, 30]. The oncological reliability of this surgical procedure is supported by the absence of local recurrence at the level of bronchial reconstruction observed in our long-term results. Given the limitation due to the small number of patients included in this series, the poor long-term survival in Stage III patients could have been negatively influenced by the high rate of cases of squamous cell carcinomas with a reduced response to adjuvant therapy. Moreover, all Stage pIIIa cases were pN2 patients, thus confirming the consolidated literature data showing N2 as the main factor affecting survival after bronchovascular reconstruction [27, 29, 30]. The present experience demonstrates that these airway reconstructions can be made without the increased jeopardy of complications. It is even more true when morbidity and mortality rates are compared with those of series including patients who undergo pneumonectomy [1]. This study has some limitations: First, the study included a small number of patients collected over a long period. The second limitation of this study is its retrospective nature. The main strength is the homogeneous series of interventions performed by the same surgical group with unmodified indications, technique and management over time. The strengths of the study are the complete long-term follow-up and the regular distribution of patients over the study period. CONCLUSION In conclusion, left lower and right middle and lower SR with reimplantation of the ULB seem to be technically feasible and oncologically adequate over the long term when the patient is carefully selected and the operation is meticulously performed. ACKNOWLEDGEMENTS We thank Marta Silvi for data management and editorial work. Conflict of interest: none declared. REFERENCES 1 Shi W, Zhang W, Sun H, Shao Y. Sleeve lobectomy versus pneumonectomy for non-small cell lung cancer: a meta-analysis. World J Surg Oncol  2012; 10: 265. Google Scholar CrossRef Search ADS PubMed  2 Ferguson MK, Lehman AG. Sleeve lobectomy or pneumonectomy: optimal management strategy using decision analysis techniques. Ann Thorac Surg  2003; 76: 1782– 8. Google Scholar CrossRef Search ADS PubMed  3 Park JS, Yang HC, Kim HK, Kim K, Shim YM, Choi YS. Sleeve lobectomy as an alternative procedure to pneumonectomy for non-small cell lung cancer. J Thorac Oncol  2010; 5: 517– 20. 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Google Scholar PubMed  19 Mathisen DJ. Right lower and middle lobe sleeve lobectomy. In: Mathisen DJ, Morse CR (eds). Thoracic Surgery: Lung Resections, Bronchoplasty . Philadelphia: Wolters Kluwer, 2015, 375– 81. 20 Gonzalez-Rivas D, Delgado M, Fieira E, Pato O. Left lower sleeve lobectomy by uniportal ideo-assisted thoracoscopic approach. Interact CardioVasc Thorac Surg  2014; 18: 237– 9. Google Scholar CrossRef Search ADS PubMed  21 Zhang X, Peng GL, Liang LX, He JX. Right, middle, and lower bronchial sleeve lobectomy by video-assisted thoracic surgery. J Thorac Dis  2013; 5: S277– 9. Google Scholar PubMed  22 Fan JQ, Yao J, Chang ZB, Wang Q, Zhao BQ. Left lower sleeve lobectomy and systematic lymph node dissection by complete video-assisted thoracic surgery. J Thorac Dis  2014; 6: 1826– 30. Google Scholar PubMed  23 Okada M, Tsubota N, Yoshimura M, Miyamoto Y, Matsuoka H, Satake S et al.   Extended sleeve lobectomy for lung cancer (the avoidance of pneumonectomy). 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Google Scholar CrossRef Search ADS PubMed  28 Pagès PB, Mordant P, Renaud S, Brouchet L, Thomas PA, Dahan M et al.  ; Epithor Project (French Society of Thoracic and Cardiovascular Surgery). Sleeve lobectomy may provide better outcomes than pneumonectomy for non-small cell lung cancer. A decade in a nationwide study. J Thorac Cardiovasc Surg  2017; 153: 184– 95.e3. Google Scholar CrossRef Search ADS PubMed  29 Deslauriers J, Grégoire J, Jacques LF, Piraux M, Guojin L, Lacasse Y. Sleeve lobectomy versus pneumonectomy for lung cancer: a comparative analysis of survival and sites or recurrences. Ann Thorac Surg  2004; 77: 1152– 6; discussion 1156. Google Scholar CrossRef Search ADS PubMed  30 Ludwig C, Stoelben E, Olschewski M, Hasse J. Comparison of morbidity, 30-day mortality, and long-term survival after pneumonectomy and sleeve lobectomy for non-small cell lung carcinoma. Ann Thorac Surg  2005; 79: 968– 73. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2018. Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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European Journal of Cardio-Thoracic SurgeryOxford University Press

Published: Jan 17, 2018

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