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Ann Thorac Surg 2005;80:1224-1230
© 2005 The Society of Thoracic Surgeons

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Original article: General thoracic

Pulmonary Resection After High-Dose and Low-Dose Chest Irradiation

^a Department of Surgery, Division of Cardiothoracic Surgery, Birmingham, Alabama USA
^c Department of Radiation Oncology, University of Alabama at Birmingham (UAB), Birmingham, Alabama USA
^b Department of Epidemiology, UAB School of Public Health, Birmingham, Alabama USA
^d Department of Biostatistics, Birmingham, Alabama USA
^e Birmingham Veterans Administration Hospital, Birmingham, Alabama

Accepted for publication February 28, 2005.

^_* Address reprint requests to Dr Cerfolio, Division of Cardiothoracic Surgery, University of Alabama at Birmingham, 1900 University Blvd., THT 712, Birmingham, AL 35294 (Email: robert.cerfolio{at}ccc.uab.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 purpose of this study is to assess the safety and efficacy of pulmonary resection after low and high dose neoadjuvant radiotherapy with concurrent chemotherapy.

PATIENTS AND METHODS: A retrospective cohort study using an electronic prospective database from January 1998 to August 2004. All patients had N2, stage IIIa, nonsmall cell lung cancer, and received neoadjuvant carboplatinum-based chemotherapy with similar doses. In addition, some patients received high-dose chest radiation (HD) equal to or greater than 60 Gy and were compared with those who received low-dose radiation (LD) less than 60 Gy. All bronchial stumps were buttressed with an intercostal muscle.

RESULTS: There were 104 patients, 50 in the LD group and 54 patients in the HD group. Median dose of radiation was 45 Gy (range 35–50.4) in the LD group and 60 Gy (range 60–66.7) in the HD group. Complete pathologic response rate was 10% compared to 28% favoring the HD group (p = 0.04). Median length of stay for both groups was 4 days and the ICU was avoided in 74%. Major morbidity and mortality rates were similar: 8% compared to 9% and 2% compared to 3.7% for the low and high dose groups, respectively. Pneumonectomy was a significant risk factor for morbidity (OR = 17.0).

CONCLUSIONS: Pulmonary resection after preoperative chest radiation is safe even after 60 Gy or higher. Sixty or higher may afford an increase in complete pathologic response and it does not seem to increase morbidity or mortality. However, if pneumonectomy is known to be required we prefer to avoid neoadjuvant radiotherapy and use chemotherapy alone.

	Introduction

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The treatment of nonsmall cell lung cancer (NSCLC) depends on the stage. The preferred treatment for many patients with resectable, biopsy proven N2 disease is neoadjuvant therapy and then restaging. If the N2 node(s) that initially harbored cancer is rendered benign (downstaged) resection is often offered in selected patients. Some prefer the use of preoperative radiotherapy concurrent with chemotherapy in these patients over chemotherapy alone [1, 2]. Patients who undergo complete R0 resection and are pathologically N2 negative have improved survival [3–5]. Moreover, those with a complete pathologic response (CR) have even greater survival [6]. The addition of neoadjuvant radiotherapy to concurrent chemotherapy may increase the rate of complete pathologic response. However, some reports of high dose neoadjuvant radiotherapy have shown increased complication rates and thus preoperative radiotherapy has usually been delivered in doses between 30 and 45 gray [7]. We along with only a few other centers have used higher "curative" doses of radiation in a preoperative setting. Not only may there be a higher CR rate, but if patients return after neoadjuvant therapy and upon restaging are found to have biopsy-proven recalcitrant or residual N2 disease and are thus denied surgery, the effectiveness of their radiotherapy has been maximized. If lower doses are used and surgery is not offered, the completion of additional radiotherapy is less effective secondary to the delay of the restaging process. We report our results in two groups of patients with N2, stage IIIa NSCLC who underwent neoadjuvant radio-chemotherapy. One group received low-dose radiation (LD) defined in this series as less than 60 Gy and the other received high-dose radiation (HD) defined as 60 Gy or higher.

	Patients and Methods

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Patients
This is a retrospective cohort study using an electronic prospective database. From January 1998 to August 2004 one general thoracic surgeon (RJC) preformed 6112 operations. Only those patients with biopsy proven N2, stage IIIA nonsmall cell lung cancer (NSCLC) was eligible. Only those patients who received neoadjuvant carboplatinum-based chemotherapy with concurrent radiotherapy, who after re-staging came to open thoracotomy with intent to completely resect for cure were included in this study. Patients were excluded if they were less than 19 years old, received non-carboplatinum based chemotherapy, had a time interval of greater than 12 weeks between completion of radiochemotherapy and resection, were deemed to be unfit to tolerate surgical procedure, had biopsy proven N3 or M1 disease, or did not undergo thoracotomy.

Staging
All patients were staged using computed tomography with 5-mm columnated slices of the chest and upper abdomen throughout this study. In addition, from January 1998 to August 2002 patients had dedicated positron emission tomography using flourodeoxyglucose F-18 (FDG-PET). FDG-PET was performed on a dedicated ECAT EXACT scanner (CTI, Knoxville, TN) until August 2002. After this date patients were staged using an integrated PET-CT scanner on a GE Discovery LS PET-CT Scanner (Milwaukee, WI). For both studies patients were asked to fast for 4 hours and then received 555 MBq (15mCi) of FDG intravenously followed by FDG-PET after 1 hour. The scans were performed from the skull base to mid-thigh level. The most recent CT scan of the chest was available for visual correlation. Maximum SUV (maxSUV) was determined by drawing regions of interest (ROI) on the attenuation corrected FDG-PET images around the primary tumor. It was then calculated by the software contained within the dedicated PET or integrated PET-CT scanner.

Patients were meticulously staged. All suspicious N2, N3 or M1 areas on CT scan and/or on FDG-PET scan (maxSUV > 2.5) were biopsied prior to pulmonary resection. Mediastinoscopy was used to biopsy suspicious lymph nodes in the paratracheal area (stations 2R, 4R, 2L, and 4L) and proximal subcarinal (7) stations and endoscopic transesophageal ultra-sound was used to biopsy suspicious posterior aortapulmonary window nodes (5), subcarinal (7), periesophageal (8), and inferior pulmonary ligament nodes (9) [8]. Patients with suspected M1 disease in the liver, adrenal, or contralateral lung underwent biopsy to prove or disprove M1 cancer. If the bone or brain was suspected to harbor metastases, MRI was considered the standard reference. If patients had biopsy proven N3 or M1 disease they were excluded from this study. Only patients with N2 disease were included in this study.

Neoadjuvant chemotherapy was given using carboplatinum-based chemotherapy. Various regimens of both chemotherapy and radiotherapy were used because many patients received their therapy close to their home. After the completion patients were meticulously restaged. If they had an EUS-FNA that proved N2 disease initially it was repeated and if the patient had recalcitrant N2 disease resection was not offered. If mediastinoscopy initially proved N2 disease it was not repeated. If restaging in these patients suggested no other metastatic sites then thoracotomy was performed and the initially involved node was sent for frozen. Resection was performed if the node was now negative. If there was only microscopic disease and the primary could be resected with a lobectomy, in selected patients lobectomy was performed but if pneumonectomy was required resection was not performed. All operative procedures were performed by one general thoracic surgeon. Complete thoracic lymphadenectomy was performed in patients who underwent complete resection. Bronchial stumps were covered in all patients using an intercostal muscle flap that is harvested prior to chest retraction using a cautery so it is devoid of periosteum (as shown in Fig 1). Pathologic review was performed via standard techniques and immuno-histochemical staining was employed when appropriate. Pathologic complete response was defined as no viable cancer cells seen on any of the resected specimen or any of the resected lymph nodes. The pathologic stage was assessed using the 1997 updated international staging system [8].

View larger version (45K): [in this window] [in a new window]   Fig 1. Intercostal muscle (ICM) flap harvested from in between the fifth and sixth ribs during a right thoracotomy. (Reprinted from Ann Thorac Surg, 80, 3, Cerfolio et al, p. 1018, Copyright (2005), with permission from The Society of Thoracic Surgeons.)

Definitions of Morbidity and Mortality
All patients were assessed each day in the hospital and complications were recorded using an electronic prospective database. All complications were recorded. They were divided as major complications (which included any problem that delayed patient discharge) and included persistent air leak with discharge on a Heimlich valve or portable pleural device or other major complications that did not delay discharge. Minor complications were also recorded and included transient atrial arrhythmias, urinary retention, and mild confusion. Operative mortality was defined as any death prior to discharge or within 30 days of surgery.

Follow-Up for Survival and Disease Recurrence
Patients were followed for cancer recurrence and survival. Follow-up data was obtained every 3 months for the first 2 years and every 6 months afterwards. A chest roentgenogram was performed every 3 months, a chest CT with intravenous contrast every 6 months. In addition, if patients became symptomatic appropriate testing (ie, bone scan, brain scan) was performed as well. Information was obtained using clinic letters, hospital computer information systems, treatment updates, social security death index, telephone calls, and letters from oncology clinics and other physicians. Patients who were still alive at the end of our study were censored. Disease free survival was measured only for those who underwent complete R0 resection. The University of Alabama at Birmingham's institutional review board approved both the electronic prospective database used for this study and this trial.

Statistics
A univariate analysis was performed to assess for differences amongst patient characteristics and risk factors in the low and high dose radiation groups. Significant factors were entered into a forward, step-wise regression analysis. A Chi-squared analysis was used for discrete variables, with p less than 0.05 according to two-tailed Fisher exact test used to select factors with potential significance. Generalized linear model (GLM) analysis of variance (ANOVA) was used to evaluate discrete nondichotomous variables. For continuous variables, the Student t test or the Mann-Whitney U test was used to compare means for non-normally distributed variables. Survival was determined using Kaplan-Meier and Cox Proportional Hazards statistics. All comparisons were two-sided with a p value of less than 0.05 used to indicate statistical significance. All statistical analysis was performed using SAS v. 8.02 (SAS Institute, Cary, NC).

	Results

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Patient Characteristics
The characteristics of the 104 patients in this study are shown in Table 1. The groups are similar for age, gender, type of pulmonary resection, and intervals between chemoradiotherapy and resection. The surgical outcomes are shown in Table 2. It shows that the groups are similar for histology and hospital length of stay. However, patients in the high dose radiation group had a statistically significant higher complete pathologic response rate (CR) as compared to patients who received low dose radiation (p = 0.04). Patients with a pathologic CR were 3.5 times as likely to have received high dose radiation. Table 3 shows similar rates and types of complications for patients in the two groups. The most common major complications were pulmonary related. Overall mortality was 3 of 104 (2.8%) and there was no statistically significant difference between the two groups for mortality.

View larger version (28K): [in this window] [in a new window]   Fig 2. Disease-free survival for patients who received high dose radiation (HD) and those that received low dose radiation (LD) (p = 0.047).

View larger version (25K): [in this window] [in a new window]   Fig 3. Kaplan-Meier survival curve for patients who received high dose radiation (HD) and those that received low dose radiation (LD) (p = 0.08).

	Comment

Top Abstract Introduction Patients and Methods Results Comment Discussion References

Pneumonectomy remains one the riskiest of all pulmonary resections. We found an extremely high increased risk OR = 17.9 (95% CI 14.1–21.8) in those patients who underwent pneumonectomy in this series. The major complication rate was 71% for right pneumonectomy and 50% for pneumonectomy. Furthermore, two of the three operative mortalities occurred in the 12 patients who underwent pneumonectomy. These results are dramatically worse than our previously reported figures for patients who underwent pneumonectomy [12] some of whom did have neoadjuvant radiochemotherapy. Fowler in 1993 [7] and Deutch in 1994 [21] also reported an increased risk for pneumonectomy after preoperative radiochemotherapy using doses of 60 Gy. Because of these findings, our preference now is to avoid neoadjuvant radiotherapy in any patients that is known to require pneumonectomy (especially a right pneumonectomy) and to use chemotherapy alone. Although it is not always possible to predict who can be completely resected with negative margins with a sleeve lobectomy, it can often be surmised based on the initial scans and/or bronchoscopy. This is true irrespective of the patient's response to neoadjuvant therapy because we favor resecting what was initially involved with cancer. Thus for those patients that have a high chance or needing a pneumonectomy, we prefer preoperative chemotherapy alone, followed by pneumonectomy if the N2 disease is downstaged.

In 2000, Pisters [6] reported a survival advantage in those patients who had a complete pathologic response after their neoadjuvant chemotherapy. In our study we found a statistically significant advantage favoring a higher complete pathologic response rate in those patients that had preoperative radiotherapy does of 60 Gy or higher. The question therefore is: will this increased CR rate translate into increased survival and thus make neoadjuvant chemoradiotherapy the preferred treatment over neoadjuvant chemotherapy alone for patients with N2 disease? Only prospective randomized trials will answer this question. In this non-randomized series, a trend toward increased disease free and overall survival was seen for patients in the HD group as compared to those who received low dose radiation. Additionally, a trend towards increased survival in patients with a CR from neoadjuvant therapy in the HD group was seen. However, neither achieved statistical significance. Since we and others have shown that resection (excluding pneumonectomy) can be safely performed with the use of intercostal muscle flaps in this highly irradiated fields it is reasonable to consider the use of high dose radiation in these patients.

Despite the fact that we found an advantage for disease-free and overall survival for those patients in the HD group, there are several limitations to this study and thus these findings must be interrupted with extreme caution. This study is non-randomized, more patients received a higher dose of radiation later in this series and this advantage achieved only borderline statistical difference. Moreover, this series did not include patients who underwent pre-operative therapy and did not come to surgery. Furthermore, it is difficult to offer an oncologic mechanism to explain increased survival from higher doses of pre-operative radiation, especially since most patients with N2 disease die from systemic, not local disease.

In conclusion, patients with stage IIIa nonsmall cell lung cancers with N2 disease, who are treated with neoadjuvant radiochemotherapy and who are downstaged can safely undergo pulmonary resection. There appears to be no increased risk using doses of 60 Gy or higher (except for those who undergo pneumonectomy). Hilar dissection can still be safely performed. This dose may offer an increase in complete pathologic response rate, but the oncologic benefits of this strategy can only be assessed with further prospective randomized multi-institutionally studies. This study, along with others, may provide the safety data and groundwork needed to perform those studies. One such study, protocol 0229 offered via the Radiation Therapy Oncology Group (RTOG) is now open for patient enrollment.

	Discussion

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DR MARK K. KRASNA (Baltimore, MD): I want to thank Dr Cerfolio really for an excellent presentation and congratulate you, Rob, on your good results as well. Two comments and then two quick questions.

The first comment, I would like to give credit to my senior partner, Dr Joe McLaughlin, for teaching us the technique of harvesting the intercostal muscle bundle in the chest. I know we shared that with Cerf many years ago, and I know he does it routinely, as do we. It is an excellent technique that can be done just like you would taking down the IMA.

The other comment is that not all radiation therapy is equal. I think it is extremely important, and I know Dr Cerfolio is doing this, to work closely, hand-in-hand, with the radiation oncologist and the medical oncologist. To deliver the high dose radiation requires very careful attention to the portals. We use a technique called IMRT for high dose therapy with hyperfractionation radiation. In order to do this routinely, you cannot just assume that any patient coming in from the community with 60 Gy can be treated with these results. So that is, I guess, a caution.

Two quick questions, Rob. Number one, can you explain to us a little the breakdown of those pateints who have had mediastinoscopy and/or EUS? Not all of us perform EUS-FNA. How did you determine in that case that patients were in fact N2 versus N3? I think that is an important issue.

My last question is regarding your final results in terms of the pathology. I was a little surprised when I saw the abstract that your path response rate was so low, quite frankly. Is it possible that your pathologist was not using an accepted international criteria to identify residual disease? I guess a secondary question is, would you have data for us on the mediastinal lymph node clearance. The mediastinal path response in all the previous data from Sugarbaker and from some of the other intergroup studies has been the important predictor.

Again, I really enjoyed your paper.

DR CERFOLIO: Thank you very much, Dr Krasna. As I mentioned in the talk, I learned this technique from Dr Sonnet, who used to be in your group at the University of Maryland. He presented this in Disney World at the Southern a few years ago—I talked to him after his presentation and started using intercostal muscle flaps the next day. I think that was in 1998 or '99 and the paper was published a year later. It is a wonderful technique and provides a reliable flap and it can be harvested in three minutes. Interestingly, there is also the benefit of decreasing the pain of thoracotomy that we have just proven in a prospective randomized trial that we just closed early.

You mentioned the type of radiation, and that is critical. You will see in this series the majority of our patients did not receive their radiotherapy at UAB because a lot of people travel to get their operation, but I think the fact that it is hyperfractionated is important—and of course at the University we use IMRT as well.

Your other question concerns the N2 or N3 nodes and that is critical. I think one of the advantages we have is this is all done with one surgeon—we have a consistent algorithm for all patients—we rule out N3 disease in any patient that has a CT scan or a FDG-PET that suggests it is positive. That node gets biopsied via EUS-FNA or a med. The advantage of proving N2 by EUS-FNA is that it is safe and reliable and can be repeated with high accuracy, as opposed to repeat mediastinoscopy—we are assessing the accuracy of repeat EUS-FNA in another study we are doing right now.

DR KRASNA: Sorry, Rob, let me just clarify that. So if the repeat EUS-FNA was negative, did you accept that or did you go ahead and do a mediastinoscopy?

DR CERFOLIO: It depends—if the initial node was proven by EUS-FNA we rely on it to clear it after neo-adjuvant therapy—but if the 2 and 4 are now suspicious on CT or FDG-PET and the patient did not have a med initially he would get both—we clear all the suspicious N2 nodes and try to save the med for restaging. If the patient had a previous med we would not repeat it and would rely on the repeat EUS-FNA to assess the 6, 7, 8, and 9, and then open thoracotomy to remove the paratracheal and wait for frozens. We have an article in JCTVS on the accuracy of repeat FDG-PET for these nodes. But I did not do a mediastinoscopy on those patients unless we questioned the paratracheal nodes.

DR KRASNA: So I would just suggest that for the manuscript it would be very interesting to see of those patients, were there any who were false negatives, meaning at thoracotomy and resection were there positives?

DR CERFOLIO: There was one patient who was falsely negative in the subcarinal station. EUS said it was negative, but the patient had microscopic disease.

And your final question was about complete response rate. Our pathologists I think looked very, very carefully at these, and if they found any microscopic disease, we considered it a T1 lesion, but there were a lot of patients with microscopic disease that may have been defined by others as a CR.

	References

Top Abstract Introduction Patients and Methods Results Comment Discussion References

 

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