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Ann Thorac Surg 2005;80:418-422
© 2005 The Society of Thoracic Surgeons

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Original article: General thoracic

Low Morbidity and Mortality for Bronchoplastic Procedures With and Without Induction Therapy

Department of Surgery, Duke University Medical Center, Durham, North Carolina

Accepted for publication February 18, 2005.

^_* Address reprint requests to Dr Burfeind, Box 3305, Duke University Medical Center, Durham, NC 27710 (Email: burfe001{at}mc.duke.edu).

Presented at the Fifty-first Annual Meeting of the Southern Thoracic Surgical Association, Cancun, Mexico, Nov 2–4, 2004.

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
BACKGROUND: The safety of bronchoplastic procedures after induction chemoradiotherapy is uncertain. This study examines short- and long-term outcomes after bronchoplastic procedures with and without induction therapy.

METHODS: Between January 1997 and September 2004, more than 1,300 anatomic pulmonary resections for cancer were performed at a single institution. Of these, 73 patients required either sleeve lobectomy (57) or bronchoplasty (16), and were retrospectively analyzed. Nineteen patients (26%) received induction therapy; 15 received chemotherapy and radiation therapy and 4 received chemotherapy alone. Fifty-four patients underwent the bronchoplastic procedure without induction therapy. Mortality and early and late morbidity were analyzed.

RESULTS: Mean follow-up was 25 months. Histology was nonsmall cell cancer in 62 (85%), carcinoid in 8 (11%), and renal cell cancer, schwannoma, and mucoepidermoid cancer in 1 patient each. There were 2 (2.7%) 30-day deaths, both in the group not receiving induction therapy. Of the surviving 71 patients, 70 had functional reconstructions at last follow-up. The overall 30-day complication rate was 30% (19 of 54) in patients not receiving induction therapy (no bronchopleural fistulas) and 42% (8 of 19) occurring in those receiving induction therapy (1 bronchopleural fistula). The long-term complication rate was 20% (11 of 54) among patients not receiving induction therapy and 5% (1 of 19) among those receiving induction therapy (completion pneumonectomy). There were no bronchovascular complications. Interventional bronchoscopy was required in 7 patients not receiving induction therapy, and was required in none of the patients receiving induction therapy.

CONCLUSIONS: Anatomic pulmonary resections utilizing bronchoplastic techniques can be performed with low morbidity and mortality rates even after induction therapy.

	Introduction

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First described by Sir Price Thomas [1], bronchoplastic techniques involve removal of a lobe in continuity with all or part of its corresponding main stem bronchus. Bronchial continuity is then reestablished with primary closure, in the case of bronchoplasty, or end-to-end anastomosis, in the case of sleeve lobectomy. Sleeve lobectomy, while initially utilized in patients with impaired pulmonary function, is currently the procedure of choice in anatomically suitable patients regardless of whether they would tolerate a larger resection [2]. Many patients with central tumors or locally advanced lung cancer, who are candidates for sleeve resection, are also being considered for induction therapy. Few series are available in the literature describing the potential morbidity and mortality associated with sleeve lobectomy after induction therapy [3–5]. This case series attempts to assess the morbidity and mortality associated with bronchoplastic lung resections both with and without induction therapy.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
Between January 1997 and September 2004, more than 1,300 anatomic pulmonary resections for cancer were performed at Duke University Medical Center. Seventy-three (5.6%) of these resections were either sleeve lobectomies (57 patients) or bronchoplasties (16 patients) and are the subject of this retrospective consecutive case series. All patients with malignant diagnoses were included. Three patients who underwent sleeve resection for benign etiologies during this time frame were excluded. Primary endpoints included 30-day or in-house death, early morbidity (<30 days), and late morbidity (>30 days). Patients were typically followed up by the operating surgeon for at least 5 years postoperatively. Deaths were cross-referenced with the National Social Security Death Index. The only statistical comparisons performed were for categorical rates of death and early complications (composite). These comparisons were done using Fisher’s exact test, and the null hypothesis was rejected at a p value of 0.05 or less.

The anatomic distribution of sleeve resections included 35 right upper lobe sleeve resections, 1 right middle lobe sleeve resection, 7 right lower lobe sleeve resections, 9 left upper lobe sleeve resections, and 5 left lower lobe sleeve resections. Fourteen patients had bronchoplastic closures after lobectomy.

Of the 73 bronchoplastic resections, 19 patients (26%) had received induction therapy; of them, 15 received chemotherapy and radiation therapy and 4 patients received chemotherapy alone. The induction therapy group was composed of 14 sleeve resections and 5 bronchoplasties. Table 1 illustrates the induction therapy given as well as its indication and time to surgery. Fifty-four patients underwent the bronchoplastic resection without induction therapy.

Pulmonary resections were performed by serratus sparing posterolateral thoracotomies. Restaging was routinely performed in patients who received induction therapy secondary to N2 disease. Bronchial margins were checked by intraoperative frozen section. Bronchial anastomoses were performed using interrupted 4–0 braided absorbable sutures and were checked for air leaks by inflating the lung while submersed in saline. Vascularized flaps, detailed in Table 1, were commonly employed to cover the anastomosis and to separate it from the pulmonary artery. Flexible bronchoscopy was performed at the conclusion of the procedures to ensure a patent anastomosis and to suction blood or secretions. Every effort was made to extubate the patients in the operating room. Thoracic epidural catheters were used liberally.

	Results

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
The mean age of patients undergoing bronchoplastic resection in this series was 58 years (range, 11 to 78). Sixty percent were male (44 of 73). The mean follow-up duration was 25 months (median, 17; range, 0.5 to 93). Histology revealed that there were 62 nonsmall cell cancers (85%), 8 carcinoid tumors (11%), and 1 each of renal cell cancer, schwannoma, and mucoepidermoid cancer. No patient left the operating room with a positive onchial margin. Staging was done according to the most recent revision of the TNM classification [6]. The distribution of pathologic stages among nonsmall cell cancers is depicted in Figure 1. The majority of tumors were T2N0 (24), T3N0 (19), or T2N2 (14). There were 3 stage IV patients, 1 with a small tumor nodule in another lobe and 2 with prolonged survival after isolated metastasis resection (1 brain and 1 femur).

View larger version (19K): [in this window] [in a new window]   Fig 1. Pathologic stage of the subset of patients with nonsmall cell lung cancer, n = 62.

	Comment

Top Abstract Introduction Patients and Methods Results Comment Discussion References

Bronchoplastic resections are typically more technically challenging than pneumonectomy. Tedder and associates [8] reported a metaanalysis of sleeve resections in 1992 and found that 30-day mortality was 5.5%, the incidence of pneumonia was 10%, and the incidences of bronchopleural fistula and bronchovascular fistula were 3% and 2.5%, respectively. Anastomotic complications can contribute to all of these negative outcomes and have been associated with pathologic N2 status and positive bronchial margins [9, 10].

Treatment of locally advanced (2B through 3B) lung cancer often employs neoadjuvant treatment protocols before surgery. The results of combined modality therapy have been encouraging, with some patients achieving long-term survival [11, 12]. A subset of these patients with locally advanced lung cancer, who are candidates for an induction protocol, will be candidates for bronchoplastic resection. The surgeon must balance the known mortality and morbidity of pneumonectomy (especially right pneumonecotmy) after induction therapy with the growing body of evidence surrounding bronchoplastic resections after induction therapy [13, 3–5].

Of the potential complications associated with bronchoplastic resections after induction therapy, anastomotic complications are the most important. Preoperative chemoradiotherapy adversely affects mucosal blood flow and healing, prompting recommendations to protect anastomoses with well-vascularized flaps [14]. In this series, there was one bronchopleural fistula after induction therapy. This patient initially underwent a right upper lobectomy and resection of the lateral wall of the right mainstem bronchus to achieve a negative microscopic margin. The resulting defect was closed primarily and covered with an intercostal muscle flap. Repair of this bronchopleural fistula required completion pneumonectomy. The overall rate of bronchopleural fistula in this series was 1.3%, and the rate in the induction therapy group was 5.2% (1 of 19). Both of these compare favorably with the rate of bronchopleural fistula after pneumonectomy, but highlight the fact that despite adequate flap coverage, a high index of suspicion needs to be maintained for this complication in patients receiving bronchoplastic resections [15]. In the series by Rendina and coworkers [3] of 27 patients undergoing chemotherapy alone followed by sleeve resection, there were no anastomotic complications. Additionally, in the study by Veronesi and colleagues [4] of 55 sleeve resection patients, 27 of whom had chemotherapy with or without radiation therapy, there was only one bronchopleural fistula in the group not receiving induction therapy. There were no bronchovascular complications in this current series. This is particularly important given that the incidence has been reported to be as high as 2.5% and that patients rarely survive this catastrophe.

The overall mortality rate in this study is comparable with that of other studies of bronchoplastic procedures, and in fact compares favorably with the national 30-day rates for standard lobectomy [16]. There were no 30-day deaths in the group of patients who received induction therapy, and the 2 deaths in the no induction therapy group were not related to anastomotic problems (1 stroke and 1 myocardial infarction). With careful selection of patients, bronchoplastic resections can be performed with acceptable mortality rates.

Early morbidity was 37% in this series and was not significantly different between groups receiving or not receiving induction therapy. The majority of early morbid events were due to atrial arrhythmias, none of which resulted in significant long-term disability (no obvious myocardial infarctions, although enzymes were not measured in all cases). The overall low rate of major postoperative complications is reflected in the median hospital stay of 5 days for both groups. The overall rate of pneumonia was particularly low at 1.3%. This finding may be an artifact due to the relatively small number of patients, but we believe is in part due to aggressive pulmonary toilet (epidurals, early extubation and ambulation, and bedside bronchoscopy for secretions, if necessary).

Late morbidity mainly consisted of the need to return to the operating room for interventional bronchoscopy. Patients typically re-presented between 3 and 15 months postoperatively with shortness of breath and chest radiographic findings of lobar collapse. Findings at bronchoscopy included granulation tissue or narrowing at the anastomosis in 5 patients, and anastomotic recurrence of lung cancer in 2 patients. Interventions for benign stenoses included balloon dilation, laser destruction of granulation tissue, and stenting. Both patients with anastomotic recurrences were stented and received photodynamic therapy, the one at 12 months and the other at 15 months.

There are notable limitations to this study. First, the retrospective nature of the study limits our ability to determine causation of any of the postoperative variable examined. Second, the relatively small number of patients limits the usefulness of statistical analysis. As such, multiple statistical comparisons between groups were avoided. The overall finding that induction therapy did not change the postoperative courses of patients undergoing bronchoplastic resections seems valid.

In summary, the results of this retrospective study suggest that bronchoplastic resections can be performed with acceptable mortality and morbidity even after induction therapy. This study adds to the growing literature confirming this finding. As larger numbers of patients undergo bronchoplastic resections after induction therapy and as they are followed up for longer periods of time, meaningful comparisons between stage-specific survivals will be performed.

	Discussion

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 
DR DANIEL L. MILLER (Atlanta, GA): Doctor Burfeind, I would like to congratulate you on an excellent presentation and thank you for supplying me with the manuscript before the meeting. I have one comment.

In regard to your pulmonary complications, you only had 1 pneumonia out of 73 patients. I think that is an incredible record. We have a lot of problems in regard to retained secretions and so forth, and I wish you would comment about your pulmonary hygiene afterward, especially in regard to complications such as number of bronchoscopies that were required, readmission to the intensive care unit, how many patients were readmitted for pulmonary complications. I think when you look at a small series like that you really have to expand the data in regard to those complications, because that is what keeps our patients in the hospital and gives us the most trouble.

And then also too I would like for you to comment briefly on the 26% of patients who had a bronchoplastic procedure, such as a wedge of a bronchus and so forth, and, as you know, that is one of the cases that got you into trouble in the induction group that you had to do a completion pneumonectomy on that. And then also I would like for you to comment again about your little bit higher rate of interventional bronchoscopy performed after the procedure.

DR BURFEIND: Thank you, Dr Miller. Well, I think our rate of pneumonia is low and may be an anomaly in this series. The charts were reviewed pretty carefully, so I am confident that this represents the true rate of pneumonia in our series. I think this is reflected in our median length of stay, 5 days. The longest length of stay was 16 days in this entire series. We didn’t have as many pulmonary complications as might have been anticipated. Again, some of that may just be because of the small number and some of it may be from the aggressive pulmonary toilet.

I think it is probably standard among many people, but we try and extubate everyone in the operating room. We also use epidurals in everybody that we can, get patients up and walking the day after surgery, and certainly if there is any compromised pulmonary function or inability to clear secretions, they get a bronchoscopy. There were multiple bedside bronchoscopies performed in this series. I don’t have the exact number, but it was used liberally.

DR MALCOM M. DECAMP (Boston, MA): I enjoyed that very much. I had a couple of questions and a comment. I think one of the things that we fear in doing bronchoplastic procedures with induction therapy is the radiation. I don’t think many of us are as worried about the chemotherapy aspects of treatment. It is the issue of bronchial healing after radiation, in those patients that are much more likely to have an aggressive mediastinal dissection as well, which further devascularizes the anastamosis. What was the preoperative radiation dose, and do you think we really have sufficient evidence based on this very small highly selected series to say that these outcomes are equivalent?

The other question deals with the issue of local recurrence. You had two local recurrences. I believe those were after sleeves and not after the more simple bronchoplastic procedures. And you also routinely used frozen sections. Were these mucosal recurrences or were these extra bronchial recurrences that suggested lymphatic involvement?

DR BURFEIND: The second question with the recurrences, they were both in the group not receiving induction therapy, they were both sleeves, and they were both recurrences at the anastomosis.

DR DECAMP: In the mucosa?

DR BURFEIND: Right, not extrinsic. And no patients left the operating room initially with positive margins. Everyone was resected to negative margins.

DR DECAMP: That is a little higher local recurrence rate than we would expect in early stage node negative lung cancer. We lose patients to brain metastases but rarely to local disease.

DR BURFEIND: In the Tedder paper from 1992, they looked at local recurrence, and it was 7% to 10%. Again, that is a older meta-analysis of data and may not apply right now. There were two local recurrences in our series.

DR DECAMP: And the radiation dose?

DR BURFEIND: The most common dose of radiation was 45 Gy. Most of the patients within that, about 11 of the 19, were treated on an in-house protocol that used carboplatinum, navelbine, and concurrent 45 Gy of radiation. There were 2 patients who were treated with full-dose radiation therapy (50 Gy and 86 Gy). They were actually treated elsewhere with definitive therapy and then came back later to us and got resected.

DR ROBERT J. CERFOLIO (Birmingham, AL): Excellent presentation and results. Tell us about how you covered the bronchus. Was it with an intercostal muscle flap?

DR BURFEIND: This was a complete mix of flaps based on surgeon preference. One of the surgeons used intercostal muscle flaps exclusively, and the other two surgeons who did most of these cases did things slightly differently; pedicled pericardial fat was a very common covering flap and azygous vein was occasionally used.

DR CERFOLIO: When an intercostal muscle flap was used, was it taken down with a Bovie so it was devoid of periosteum, so it does not calcify over time. And as importantly, was it harvested prior to chest retraction?

DR BURFEIND: Typically they were harvested prior to chest retraction in these cases. They were not intentionally devoid of periosteum, but it is important to note that these were not circumferential wraps of the anastomosis, more to sort of cover it anteriorly and then separate it from the pulmonary artery.

DR CERFOLIO: I think if you take it down with a Bovie and it is devoid of periosteum, you can circumferentially wrap, because it will not calcify—however, I do not recommend it—it is best to probably never circumferentially wrap any anastomosis with any flap.

DR BURFEIND: We agree.

	References

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 

1. Price Thomas C. Conservative resection of the bronchial tree J R Coll Surg Edinb 1955;1:169-186.
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6. Mountain CF. Revisions in the international system for staging lung cancer Chest 1997;111:710-717.
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