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Ann Thorac Surg 2003;75:237-242
© 2003 The Society of Thoracic Surgeons

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Original article: general thoracic

Limited resection for non–small cell lung cancer: observed local control with implantation of I-125 brachytherapy seeds

^a Division of Cardiothoracic Surgery, New England Medical Center and Tufts University School of Medicine, Boston, Massachusetts, USA
^b Department of Radiation Oncology, New England Medical Center and Tufts University School of Medicine, Boston, Massachusetts, USA

Accepted for publication July 24, 2002.

* Address reprint requests to Dr Daly, 88 East Newton St, B402, Boston Medical Center, Boston, MA 02118, USA.
e-mail: benedict.daly{at}bmc.org

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
BACKGROUND: Limited resection for lung cancer has been associated with a relatively high incidence of local recurrence. This retrospective study evaluates the impact of implanting radioactive iodine-125 (¹²⁵I) seeds along the resection margin in these patients.

METHODS: Thirty-three patients with lung cancer who were not candidates for lobectomy or pneumonectomy underwent a limited resection of 35 primary non–small cell lung cancers. ¹²⁵I brachytherapy seeds were implanted along the resection margin to reduce the risk of local recurrence. Survival using the Kaplan-Meier method and sites of recurrence were documented. Follow-up ranged from 20 to 98 months (median, 51 months).

RESULTS: The 5-year survival was 47% for all patients. For patients with T1N0 tumors, it was 67%, and for patients with T2N0 tumors, it was 39%. However, the cancer-specific survivals were 77% and 53% for patients with T1N0 and T2N0 tumors, respectfully. Ten patients experienced recurrence, with two local (at the resection margin) and six regional recurrences (five mediastinum, one chest wall). Both local recurrences and one regional recurrence occurred in the 19 patients with T1N0 tumors.

CONCLUSIONS: ¹²⁵I seed implantation along the resected margin for compromised patients undergoing limited resection of lung cancer results in a relatively low incidence of local recurrence and may prolong survival.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Surgical resection is the definitive treatment for early-stage non–small cell lung cancer (NSCLC); lobectomy remains the procedure of choice [1–3]. Lesser resections have been associated with an increased risk of local recurrence, even for small peripheral tumors [4]. However, limited resection is viewed as an acceptable alternative treatment for patients with poor physiologic reserve or of advanced age [5, 6]. External beam radiation therapy (XRT) has been used successfully to reduce the risk of local recurrence in these patients [7]. However, XRT further reduces pulmonary function because it generally requires the beam to pass through normal lung to reach the target lesion. Interstitial brachytherapy (BxT) has been used with equivocal results as an alternative to, or in conjunction with, XRT to improve local control in resected patients with close or positive margins [8, 9]. d’Amato and colleagues recently reported favorable results using a BxT technique to implant ¹²⁵I seeds for improving local control in patients undergoing thoracoscopic wedge resection for peripheral stage I lung cancers. Their follow-up in 14 patients ranged from 2 to 12 months [10]. In this report, we present ¹²⁵I BxT results in 33 patients, with follow-up ranging from 20 to 98 months (median, 51 months).

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Between October 1993 and September 2000, 35 consecutive limited resections were carried out in 33 patients who were deemed not to be candidates for a lobectomy or pneumonectomy. Two patients with second malignancies were considered twice. There were 19 men and 16 women, with a median age of 69 years (range, 46 to 86 years). Thirty-two patients underwent a wedge resection, and 2 patients underwent a segmental resection. One patient with tumor extending across a fissure who could not undergo a pneumonectomy received a lobectomy and ¹²⁵I seed implantation along the lung margin. We have categorized the primary indication for limited resection and associated conditions or symptoms that led to this choice of management in Table 1. Patients with a forced expiratory volume in 1 second (FEV₁) of 1.0 L or less or who had an exercise tolerance of one flight of stairs or less were categorized as having a pulmonary indication for limited resection. Patients who were limited by medically or surgically uncorrectable heart disease were considered to have a cardiac indication, and patients over 75 years who refused lobectomy or pneumonectomy for quality of life and risk issues were considered eligible. Twenty-one patients had compromised pulmonary function. The median FEV₁ in these patients was 1.02 L (range, 0.43 to 1.74 L). Six patients were compromised by significant cardiac disease. Four patients had significant ischemic coronary artery disease and 2 patients had a significant cardiomyopathy. Six patients underwent a conservative resection because of advanced age (median, 82 years; range, 78 to 86 years). Two patients had a complicating illness. One had had previous high-dose radiation to the mediastinum, and 1 had advanced cirrhosis.

Ten ¹²⁵I brachytherapy seeds embedded in polyglactin 910 suture (Amersham Health, Princeton, NJ) were spaced 1 cm center-to-center to make a radioactive strand. Strands were affixed either along the resection margin or 0.5 cm on either side of the resection margin depending on the radiation intensity of the seeds, the length of the resection margin, and the number of seeds available. In most cases, from one to three strands were affixed on both sides of the resection margin over its entire length, utilizing interrupted sutures of 3-0 silk spaced approximately 2 cm apart. Whenever an insufficient number of seeds were available to cover the entire resection margin with parallel strands, the most peripheral portion of the resection margin was affixed with a single strand, and the more central portion affixed with parallel strands on either side of the stapled margin (Fig 1). Source strength was chosen to deliver a combined radiation dose of 125 to 140 Gy at a 1-cm depth [11, 12], and averaged 0.7 mCi per seed. For a given implant, all seeds had identical source strength. Dose was calculated using the one-dimensional dosimetry formalism with the ADAC Pinnacle treatment planning software (Milipatas, CA) assuming infinite source decay. After complete lung reinflation, final dosimetry was obtained postoperatively using orthogonal radiographic films or more recently CT-based three-dimensional treatment planning (Fig 2). Unless nodal metastases were demonstrated, additional adjuvant treatment for potential hilar or mediastinal lymphatic tumor was not offered. The patient with a T2N1 tumor and the patient with a T1N2 tumor received postoperative adjuvant radiation to the ipsilateral hilum and mediastinum.

View larger version (57K): [in this window] [in a new window]   Fig 1. Portion of lung in which a wedge resection has been carried out. Each limb of the wedge resection is approximately 6 cm in length. Shown is how two 10-seed strands would be affixed to the margin. The most peripheral seeds are placed directly in the margin, and the deeper portions of the wedge have two strands of seeds affixed to the lung spaced approximately 1 cm apart or 0.5 cm from the resection margin. Simple 3-0 silk sutures are used to hold the strands in place.

View larger version (157K): [in this window] [in a new window]   Fig 2. Diagram of a three-dimensionally reconstructed brachytherapy dosimetry plan using I-125 seeds. The isodose distribution legend is at upper left, the distance scale is at right (yellow), and the average 1-cm dose distribution for this implant was about 110 Gy. In this plane, locations of some of the seeds are indicated by crossed circles.

	Results

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
There was one operative death. This occurred in a patient who had undergone a left pneumonectomy several years earlier and presented with a second primary lung cancer in the right lower lobe. He was dyspneic with minimal exertion and had an FEV₁ of 1.13L. He developed pneumonia followed by adult respiratory distress syndrome early in the postoperative period, died 13 days postoperatively, and is considered a cancer death. Nine other patients had a single complication, and 1 had multiple complications. The single complications were lobar collapse, left lung collapse, hematemesis, hemothorax (patient on heparin for prosthetic valve), supraventricular tachycardia, atrial fibrillation, acute tubular necrosis (recovered), and prolonged air leak (11 days). The patient with multiple complications (patient EL, Table 1) experienced atrial fibrillation, myocardial infarction, gastrointestinal bleeding, radial artery thrombosis requiring thrombectomy, deep venous thrombosis requiring a vena cava filter, and Clostridium difficile colitis. The mean hospital stay for all patients was 7.7 ± 2.8 days (range, 4 to 14 days).

Median survival was 45 months, with a projected 5-year survival of 47% (CI 29% to 65%). Because all patients were medically compromised, we calculated the cancer-specific survival for this group. The projected cancer-specific 5-year survival was 61% (CI 42% to 80%). For the 19 patients with T1N0 cancers, the projected 5-year survival and cancer-specific survival was 67% (CI 45% to 89%) and 77% (CI 57% to 97%), respectively, and for the 10 patients with T2N0 cancers, the projected 5-year survival and cancer-specific survival was 39% (CI 1% to 77%) and 53% (CI 7% to 99%), respectively (Fig 3). In addition to the postoperative death, there was a second patient (HO) who died in the second month after surgery with general debilitation. He is also considered a cancer death. The recurrence sites and causes of death for all patients are shown in Table 1. Five died from local or regional recurrence, 2 from systemic metastases, and 3 from both. The patient (MM) who died with a chest wall recurrence had three previous resections over an 11-year period for metachronous primary lung cancers, and had extensive adhesions at the time of her operation from a previous resection. Her chest wall recurrence occurred both at the site of her incision and along the adjacent pleura. Three patients died from cardiovascular disease, 1 patient from chronic obstructive pulmonary disease, and 3 patients from other cancers. There were no short- or long-term complications observed due to ¹²⁵I seed implantation.

View larger version (13K): [in this window] [in a new window]   Fig 3. Cancer-specific survivals for patients with T1N0 and T2N0 tumors.

	Comment

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

Because local recurrence is higher in virtually every report that compares lobectomy with limited resection, the focus of this report is local recurrence. All patients had been followed for a minimum of 20 months, with median and maximum follow-up of 51 and 98 months, respectively. In patients with T1N0M0 lung cancers undergoing definitive resection, local recurrence at the site of resection occurred in only 2 of 19 patients (10.5%). One of these recurrences occurred over 5 years after resection, and it is possible it represented a second primary cancer. However, it developed in the area of the seeds and is considered a local recurrence. The other local recurrence occurred in a patient with a peripheral 1.5-cm adenocarcinoma. There were five regional recurrences. The only one occurring in a patient with a T1N0 tumor occurred in a patient with a peripheral 2.9-cm adenocarcinoma in the left upper lobe and an FEV₁ of 0.7 L. She did not have mediastinoscopy, and lymph node sampling was not performed to minimize the invasiveness of her procedure. Three other regional recurrences developed in patients with T2N0M0 lung cancers and one in a patient with a T3N0M0 lung cancer. Three of these regional recurrences were in the mediastinum and one was in the chest wall. None of these 4 patients had undergone a mediastinoscopy or nodal sampling. In patients with stage IB tumors and higher, the risk of regional recurrence increases. Every effort should be made to stage the hilar and mediastinal lymph nodes in these patients, and a limited resection should be avoided whenever possible.

These results suggest that limited resection is a reasonable alternative to nonoperative management of lung cancers for compromised patients, particularly those patients with stage IA lung cancers. The implantation of ¹²⁵I seeds is effective in reducing recurrence at the resected lung margin. ¹²⁵I seeds are not effective in preventing mediastinal recurrence, as four mediastinal recurrences were observed (10%). Based on this small series, it is clear that in most cases mediastinoscopy should be performed even with a negative chest CT and PET scan because lobectomy is not an option in the majority of these patients. In addition, mediastinal lymph node sampling or dissection should be carried out whenever feasible because occult mediastinal lymph node metastases may be uncovered, and some of these patients would be candidates for adjuvant limited field radiation.

The Lung Cancer Study Group (LCSG) conducted the first prospective, multiinstitutional randomized study to compare lobectomy with intentional limited resection for T1N0 NSCLC [1]. Their analysis revealed a threefold increase in locoregional recurrence with limited resection (17.2%) compared with lobectomy (6.4%), but no difference in distant recurrence (13.9% vs 12%). Limited resection was associated with a 30% increase in the overall death rate and a 50% increase in the observed death rate with cancer, but when the entire group of 276 patients was considered, the observed survival differences (20% vs 30%) lost statistical significance. It should also be noted that the death rate was significantly higher in patients 60 years of age or older with a poor performance status. The only benefit seen in the limited resection group was postoperative FEV₁. Whereas the locoregional recurrence in our series was comparable to that observed by the LCSG, none of our patients underwent intraoperative nodal sampling with frozen sections. The operation was, indeed, truly limited. More aggressive preoperative or intraoperative nodal sampling to validate this approach might have identified several patients who were either not operative candidates or who would have benefited from adjuvant treatment postoperatively. Warren and Faber reported similar results [4]. They compared segmentectomy versus lobectomy in patients with stage I NSCLC and poor cardiopulmonary reserve. They demonstrated no statistical difference in 5-year survival for tumors 3 cm or smaller; the locoregional recurrence in the segmentectomy group was 22.7% versus 4.9% in the lobectomy group. The most common cause of death in both groups was distant recurrence, suggesting locoregional recurrence may not correlate with distant recurrence or 5-year survival.

The current standard of care for stage I NSCLC is lobectomy, which is associated with a survival between 40% and 75% [1, 2]. Patients treated with XRT or observation have an overall 5-year survival of 13% to 21% [13, 14]. In 1973, Jensik and colleagues demonstrated that segmental resection was an acceptable alternative to lobectomy for certain patients with peripheral tumors [15]. They achieved an overall 5-year survival of 56.4% in 69 patients undergoing curative resection over a 15-year period, with only six loco-regional recurrences. More recent studies, however, have shown that there is a significantly higher incidence of local recurrence with limited resection [1, 4, 6, 7].

To evaluate limited resection as a compromise procedure, Kodama and colleagues compared limited resection performed as a compromise procedure to limited resection as an intentional procedure and lobectomy for T1N0 NSCLC [5]. There was no significant difference in 5-year survival in the lobectomy group (88%) compared with the intentional limited resection group (93%). However, the difference was significant when compared with the compromised group (48%). Locoregional recurrence followed a similar pattern, as the difference between lobectomy (1.3%) and intentional limited resection (2.2%) was not significantly different until compared with compromised limited resection (11.8%). There were no significant differences in distant recurrence. Their data suggest that intentional limited resection with regional lymph node dissection is an acceptable alternative treatment in selected patients with T1N0 disease.

A number of approaches have been used to reduce the risk of local recurrence associated with limited resection. Miller and Hatcher reported a local recurrence rate of 35% among 20 patients with an FEV₁ of 1 L or less undergoing limited resection alone, but a local recurrence rate of only 6.25% among 32 patients undergoing limited resection followed by XRT [7]. As conventional XRT requires a large volume of lung to be irradiated to improve local control, other methods to improve local control have been studied in order to preserve functional lung volume. In a preliminary report, McGrath and colleagues compared the volume of treated lung after ¹²⁵I seed implantation with the volume that would be treated with XRT, and found that there was a decrease of approximately fivefold or greater in significantly irradiated lung compared with XRT [16]. Utilizing a thoracoscopic approach, d’Amato and colleagues applied ¹²⁵I brachytherapy to the resected lung margins of 14 patients with high-risk stage I NSCLC [10]. Although there were no reported local recurrences or cases of radiation pneumonitis, median follow-up time was limited at 7 months. Our technique furthered this approach by providing more patients and follow-up, and administering a higher radiation dose to the resected lung margin.

Lobectomy or pneumonectomy and lymph node dissection is our standard of care for patients with lung cancer because it reduces the possibility of intrapulmonary lymphatic or hilar microscopic disease from developing into the regional nodal recurrence, which continues to be a problem with any limited resection. However, some patients may not be suitable candidates for that approach. Since 1993, we have utilized ¹²⁵I seeds to reduce the risk of local recurrence at the margin of resection in patients undergoing a limited resection for lung cancer. In patients undergoing a deep wedge resection, this margin would include the hilar structures that would have been sacrificed if a lobectomy had been carried out. The regional lymph nodes, on the other hand, would not receive any significant amount of radiation.

The advantages of utilizing ¹²⁵I seeds to improve local control include cost-effectiveness in comparison to repeated application of conformal radiation, adaptation to tumor size and shape, deliverance of a higher tumor dose of radiation, sparing of normal lung tissue, and continuous irradiation over a longer period of time [17]. In this small series, combined with limited resection, acceptable survival and local control was achieved in the majority of compromised patients with stage IA disease. However, to validate this approach, the accrual of more patients with longer follow-up will be required ideally in a prospective, multicenter randomized clinical trial.

	Acknowledgments

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
This study was supported by the Edmund C. Lynch Fund at Tufts-New England Medical Center.

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Lee, W. Articles by Rivard, M. J. Search for Related Content PubMed PubMed Citation Articles by Lee, W. Articles by Rivard, M. J. Related Collections Lung - cancer