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Ann Thorac Surg 2010;89:870-875. doi:10.1016/j.athoracsur.2009.11.052
© 2010 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Microscopic Residual Disease After Resection for Lung Cancer: A Multifaceted but Poor Factor of Prognosis

Marc Riquet, MD, PhD*, Karima Achour, MD, Christophe Foucault, MD, Françoise Le Pimpec Barthes, MD, PhD, Antoine Dujon, MD, Aurélie Cazes, MD, PhD

General Thoracic Surgery and Pathology Departments, Georges Pompidou European Hospital, Paris and Cedar Surgical Centre, Boisguillaume, France

Accepted for publication November 19, 2009.

* Address correspondence to Dr Riquet, General Thoracic Surgery Department, Georges Pompidou European Hospital, 20 rue Leblanc, 75015, Paris, France (Email: marc.riquet{at}egp.aphp.fr).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Many studies focus on bronchial microscopic residual disease (R1) after resection for lung cancer, although R1 also concerns vascular and soft tissues. Our purpose was to study the R1 prognosis at different resection margins and to compare it with the prognosis for those having complete resection (R0).

Methods: We reviewed the clinical records of 4,026 patients from two centers who underwent surgery in view of cure. Despite perioperative frozen section, 216 patients (5.4%) proved R1 and were classified into seven types according to R1 anatomic site: bronchus, peribronchus, great vessels and atrium, mediastinum and pericardium, chest wall, lung tissue, and lymph nodes. Patients who were classified as R0 and R1 were compared, and R1 patients were further studied according to R1 margins.

Results: Frequency of R1 increased with the T and N values and type of resection (lobectomies, 3.3% [70 of 2,041 patients]; pneumonectomies, 8.8% [126 of 1,308 patients]; p < 10–6). Five-year survival rates for R1 patients were lower than those for R0 patients (20% versus 46%; p < 10–6), and were not modified by the degree of T and N involvement or adjuvant therapy, but were better in bronchial and peribronchial (48.4% of R1 patients) than in extrabronchial R1 (26.3% versus 15.6%; p = 0.023). Multivariate analysis confirmed R1 to be an independent factor of poor prognosis (p = 0.0008), after N, T, and age.

Conclusions: Long-term survival is possible in case of an R1 margin, but 5-year survival rates are jeopardized. Poor efficacy of adjuvant therapy and global outcome indicate advanced disease or reflect tumor cell aggressiveness, rather than surgical insufficiency, when prevention of R1 margins is guided by frozen-section examination and scrupulously respected.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The American Joint Committee on Cancer termed R0 the complete resection of non–small cell lung cancer (NSCLC) with all resection margins declared free of tumor by pathologist, R2 a macroscopic incomplete resection with gross tumor left behind, and R1 a resection with microscopic invasion of the surgical margin [1]. Microscopic residues may involve not only the bronchial stump but also vascular and soft tissues. Many studies focus on residual disease at the bronchial stump, some of them being very detailed. The most relevant were analyzed in two recent literature reviews [2, 3], whose purpose was to look for the best management in such cases with the main question being the need for reoperation. On the contrary, the publications dealing with residual disease present after surgery for other pT3 and T4 NSCLCs are few: they commonly report poor long-term results but are lacking detailed anatomic description [4–8]. Our purpose was to study the prognosis of the different patterns of residual disease at resection margins according to pathology stages and to compare the results with those of patients who underwent R0 resections during the same period.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
The clinical records of 4,026 patients who underwent complete surgery in view of cure for NSCLC between April 1984 and December 2006 in Georges Pompidou European Hospital (Paris) and Cedar Surgery Centre (Boisguillaume) were reviewed. The preoperative workup included chest roentgenogram, bronchoscopy, computed tomography scan of the chest, spirometry, lung perfusion scan, and a thorough search for distant metastases (including positron-emission tomography scan in recent years). Mediastinoscopy was performed to exclude N3 disease and to better assess N2 disease in patients included in various neoadjuvant treatment protocols (depending on different referring centers). All patients underwent a thoracotomy with segmentectomy, lobectomy, bilobectomy, or pneumonectomy and mediastinal lymph node (LN) resection. Resection margins were routinely controlled by peroperative frozen-section studies when technically feasible. The staging system was the International Staging System for NSCLC adopted in 1997 [9], and recently modified concerning the T stage [10]. The study was approved by the hospitals' ethic committees, which waived the need for informed consent. After pathology department review of tumor slides, the patients were classified into six different types of R1 according to the exact anatomic site of microscopic residual disease: bronchus, peribronchus, great vessels and atrium (T4), mediastinum and pericardium (T3), chest wall (T3), and lung tissue. We also included a seventh R1 subtype of patients with involved mediastinal LNs whose ruptured LN capsula was tightly adherent to mediastinal structures, leading us to consider that microscopic residual disease was probably left behind despite apparently perfect completeness of lymphadenectomy (LNs R1).

Both R0 and R1 patients were compared according to their epidemiology, pathology, and prognosis characteristics. The R1 patients were further studied according to the type of R1 involvement, and data were presented separately for whether neoadjuvant chemotherapy was performed or not.

Follow-up information was obtained from the hospital case records, from a questionnaire completed by the chest physician or general practitioner, or from death certificates. The main outcome was the overall survival, defined as the time interval between the date of operation and the date of death or the last follow-up visit for censored patients. The causes of death were specified when related to the NSCLC: the site of first recurrence was termed "local" when it was intrathoracic. Mean follow-up duration was 72.8 (± 48) months; and 65 patients were lost during follow-up, 5 of them with R1 resection (known survival duration of 2, 4, 5, 10, and 29 months). Univariate analysis was conducted between both populations. Actuarial survival curves were estimated by the Kaplan-Meier method. Statistical comparisons between survival distributions were made using the log-rank test. Multivariate analysis was performed using the Cox proportional hazards model for overall survival analysis. Univariate analysis used the following outcome variables: sex, age, type of surgical resection, histology, T, type of N involvement, and R. All data analyses were conducted with the two-sided test: a probability value less than 0.05 was considered as statistically significant. The statistical software used for the analysis was SEM (Anticancer Centre Jean Perrin, Clermont-Ferrand, France) [11].


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
The 5-year and 10-year survival rates of the 4,026 patients were 44.2% and 27.7%, respectively (median, 47 months). Despite common use of perioperative frozen-section studies, pathologic examination finally disclosed 216 patients (5.4%) with microscopic residual disease (R1), 3,810 patients being R0. Univariate analysis of the main prognostic factors is shown in Table 1, including R0 and R1 5-year survival rates. Both R0 and R1 patients and their characteristics are shown in Tables 2 and 3, Go and R1 patients and the type of involved margin are shown in Table 4.


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  		Table 1 Five-Year Survival Rates According to the Main Characteristics of the R0 and R1 Populations
 

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  		Table 2 Main Epidemiologic and Therapeutic Characteristics of R1 and R0 Non–Small Cell Lung Carcinomas
 

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  		Table 3 Pathology Characteristics of R1 and R0 Non–Small Cell Lung Carcinomas
 

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  		Table 4 R1 Patients According to the Localization of Microscopic Residual Disease and to Main Pathology and Therapy Characteristics
 
The frequency of R1 resection increased with the T value (T1, 2.1% [24 of 1,125 patients]; T2, 2.5% [54 of 2,085 patients]; T3, 15.8% [103 of 547 patients]; and T4, 39.2% [35 of 53 patients]; p < 10–6) and the degree of LN involvement (N0 2.3% [51 of 2,173 patients]; intralobar N1 2.5% [18 of 312 patients]; extralobar N1 6.5% [30 of 431 patients]; single-station N2 8.4% [54 of 587 patients]; multiple-station N2 17% [63 of 307 patients]; p < 10–6).

The type of surgery was different, R1 being present in 3.3% of lobectomies (70 of 2,041 patients) and 8.8% of pneumonectomies (126 of 1,308 patients; p < 10–6). Neoadjuvant therapy has been performed in 1 of 4 R1 patients. Details of therapy and pathologic diagnosis are provided in Tables 2 and 3. Diagnosis of R1 disease was more frequent in case of more advanced NSCLCs, as indicated by significantly more T3 and T4, N1 and N2, and lymphatics and blood vessels invasion. Eighty-two percent of postoperative survivors underwent adjuvant therapy (Table 2), and more precisely, 74% underwent radiation therapy. No patient underwent reoperation (mainly because of unfeasibility owing to already performed major operation and advanced stages, or more secondarily because of lung function impairment). However, reoperation should have concerned 9.5% of patients (10 of 104 patients) with bronchial and peribronchial R1 who were N0 after lobectomy: 1 of the patients was lost at follow-up after 30 months, and 4 patients were alive and disease-free at 5 years; 5 patients died at 28, 32, 43, 50, and 57 months, with only one local recurrence.

R1 resection proved to be an important factor of poor prognosis when compared with R0 (Fig 1). Postoperative deaths were twice more frequent, despite similar complication rates (Table 2); bronchial fistulas were observed in 57 of R0 plus R1 patients (1.5%), 6 of R1 (2.8%), and 3 of bronchial and peribronchial R1 (2.9%; p = 0.23). Five-year survival rates were divided by more than two. Survivorship remained as poor regardless of the degree of T and N involvement (Table 5). Five-year survival rates for R1 disease were not modified by neoadjuvant therapy (19.8%, median, 20 months versus 20.3%, median, 16 months; p = 0.76) or by adjuvant therapy (21.6%, median, 19 months versus 21.3%, median, 15 months; p = 0.87; Table 5).


Figure 1
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  		Fig 1. Comparison of 5-year survival rates between R0 (curve 1): 46%, median, 51 months; and R1 (curve 2): 20.1%, median, 17 months (p < 0.0000001).

 

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  		Table 5 Five-Year Survival Rates According to T and N for R1 and R0 Non–Small Cell Lung Carcinomas
 
Bronchial and peribronchial microscopic residues represented 48.4%, chest wall, 19.8%, great vessels and atrium, 13.8%, and LNs, 11.5% of R1 patients (Table 4). Five-year survival rates were better in case of bronchial and peribronchial R1 than in case of other R1 sites (Table 4, Fig 2). Local recurrence was observed in 15.3% of deceased R1 patients (33 of 173 patients) and in 4.4% of R0 patients (168 of 2,147 patients; p = 0.10–6). Local recurrence was observed in 19% of bronchial and peribronchial R1, 12% of great vessels and atrium R1, 22.2% of chest wall R1, and 21.5% of LNs R1 (Table 6).


Figure 2
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  		Fig 2. Five-year survival rates between bronchial and peribronchial R1 (curve 1): 26.3%, median, 22 months; lymph nodes R1 (curve 3): 10.7%, median, 10 months; and other R1 (curve 2): 15.6%, median, 16 months (p = 0.023). Survival rates between curves 2 and 3 are not significantly different (p = 0.16).

 

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  		Table 6 Local Non–Small Cell Lung Carcinoma Recurrence Observed in Patients Who Underwent R1 Resections According to Location of Residual Microscopic Disease
 
Multivariate analysis confirmed R1 resection to be an independent factor of poor prognosis (p = 0.0008), after N, age, T, type of resection, and histology.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
The concept of R1 disease is commonly associated with bronchial margin involvement. Occurrence of bronchial R1 resection was described as early as 1945 [12]. Residual tumor cells can invade the entire bronchus or be confined to a specific part of the bronchial wall. Mucosal, submucosal [12], and peribronchial [13] residues were described more than 50 years ago. The frequency of bronchial margin involvement may be as high as 13.3% [12], 14.7% [14], or 17% [15], but is generally less than 6% [3]. Several studies reported a frequency of 2.3% [16], 2.6% [17], and 2.7% [18], similar to that we observed in bronchial R1 (104 of 4,027 patients; 2.6%). That low frequency may be related to intraoperative frozen-section examination of the resection margins, but such examination does not suffice to prevent incomplete resection; false-negative rates as high as 41.7% were reported by Kaiser and colleagues [19]. The survival rates between patients with bronchial and those with peribronchial R1 disease were not different in our series, whereas the prognosis was reported to differ according to the pattern of residual disease at the bronchial resection margin since the first publications. Dysplasia and carcinoma in situ are known not to affect the prognosis [20, 21], even if deep glandular carcinoma in situ may be associated with a greater risk for early stump recurrence [22]. Such patients were not included in our study. On the contrary, we observed that N2 was more frequent (68.3% versus 37.8%; p < 10–6) in case of peribronchial R1, but without influencing the long-term prognosis. Massard and colleagues [23] underlined that the prognosis of bronchial R1 and N2 disease were not very far from being similar, which is supported by our observation. Collaud and colleagues [24] reported that peribronchial disease and margin lymphatic infiltration was clearly more common in advanced stages, but that survival also proved to be dismal when it was present in early stages. The authors suggest that this may express early systemic dissemination and argue for chemotherapy rather than for reoperation.

In effect, the discovery of microscopic bronchial residues on pathology examination raises the question of reoperation. However, pathologic and functional limitations are frequent causes of incomplete resections and are estimated to account for at least 40% of cases [25]. In our series, incompleteness of resection was significantly related to more advanced pathology stage (Tables 1, 2), explaining why reoperation was not attempted. Reoperation is more likely discussed after lobectomy in case of bronchial R1. Balasubramanian and colleagues [2] reviewed 427 papers, of which only 14 were relevant to answer this question. It appeared that further resection was an acceptable treatment option for patients with stage I or II tumors who could tolerate reoperation, and that it might improve survival. However, only four studies recommended this strategy, with the remaining papers reporting no significant differences in survival for the patients. Reoperations were few, completion pneumonectomy being performed in 9.9% (2 of 21 patients [17], 2 of 47 patients [26], and 5 of 23 patients [20]). In our series, reoperation should have hypothetically prevented only one local recurrence, if the patient had been deemed operable.

Bronchial R1 represented less than 50% of all R1 resections we performed. The most frequent other extrabronchial R1 sites were great vessels and atrium, chest wall, and LNs R1. Extrabronchial margins are often difficult to assess during operation because of too large an area of the chest wall, lung parenchyma, diffuse hilar adipose tissue, or calcifications and ribs. Chest wall and great vessels plus atrium R1 has been mentioned in some series [25, 27], without further analysis. Extrabronchial R1 is reported as a factor of poor prognosis in papers dealing with resected T4 NSCLCs [4, 5] or with mediastinal invasion [7]. R1 resection dramatically affects the outcome of patients with chest wall T3, as we observed. That microscopic tumor spread is effectively a major prognosticator, and the factor is probably underrated: in patients with poor survival rates despite tumor-free chest wall margin by histopathology examination, presence of microscopic tumor spread was demonstrated by retrospective immunohistochemistry [28]. R1 resection is frequent when tumors are invading the great vessels and atrium [8, 29], and leads to low 5-year survival rates (14.8% [8], 14% [29], percentages similar to ours). Reoperation is not commonly discussed for extrabronchial R1 because tumor spread is obviously still more important. Prognosis is very poor, and still poorer than in cases of bronchial R1 (Table 3, Fig 2). Here, too, R1 diagnosed by pathology examination, although unsuspected by frozen sections, is presenting as a factor of poor prognosis in itself. Although R1 resections are mainly observed in case of important regional tumor spread, the commonly mentioned inefficacy of adjuvant therapy (surgery, but also radiation and chemotherapy, as we also observed), may suggest a specific associated tumor cell aggressiveness.

To conclude, R1 discovered at pathology examination may concern all boundaries of the NSCLC resection. Long-term survival is possible, but 5-year survival rates remain low. Postoperative mortality, poor efficacy of adjuvant therapy, and poor global outcome may be attributable to more advanced disease and reflect greater tumor cell aggressiveness rather than surgical insufficiency.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We gratefully acknowledge the help of Dr Jacques Médioni for statistical analysis.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. American Joint Committee on Cancer (AJCC) AJCC cancer staging handbook6th ed.. New York: Springer; 2002.
  2. Balasubramanian S, Au J, Dunning J. Should lobectomy patients with microscopic involvement of the bronchial resection margin undergo re-operation to improve their long-term survival? Int Cardiovasc Thorac Surg 2005;4:531-537.[Abstract/Free Full Text]
  3. Wind J, Smit EJ, Senan S, Eerenberg JP. Residual disease at the bronchial stump after curative resection for lung cancer Eur J Cardiovasc Surg 2007;32:29-34.
  4. Yildizeli B, Dartevelle PG, Fadel E, Mussot S, Chapelier A. Results of primary surgery with T4 non-small cell lung cancer during a 25-year period in a single center: the benefit is worth the risk Ann Thorac Surg 2008;86:1065-1075.[Abstract/Free Full Text]
  5. Osaki T, Sugio K, Hanagiri T, et al. Survival and prognostic factors of surgically resected T4 non-small cell lung cancer Ann Thorac Surg 2003;75:1745-1751.[Abstract/Free Full Text]
  6. Pitz CCM, Brutel de la Rivière A, van Swieten HA, Westermann CJJ, Lammers JWJ, van den Bosch JMM. Results of surgical treatment of T4 non-small cell lung cancer Eur J Cardiothorac Surg 2003;24:1013-1018.[Abstract/Free Full Text]
  7. Doddoli C, Rollet G, Thomas P, et al. Is lung cancer surgery justified in patients with direct mediastinal invasion? Eur J Cardiothorac Surg 2001;20:339-343.[Abstract/Free Full Text]
  8. Fukuse T, Wada H, Hitomi S. Extended operation for non-small cell lung cancer invading great vessels and left atrium Eur J Cardiothorac Surg 1997;11:664-669.[Abstract/Free Full Text]
  9. Mountain CF. Revisions in the international system for staging lung cancer Chest 1997;111:1710-1717.[Medline]
  10. Goldstraw P, Crowley J, Chansky K, et al. The IASLC cancer staging project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM classification of malignant tumours J Thorac Oncol 2007;2:706-714.[Medline]
  11. Kwiatkowski F. SEM (Statistiques, Epidémiologie, Médecine): un outil de gestion informatique et statistique adapté à la recherche en cancérologie Bull Cancer 2000;87:715-721.[Medline]
  12. Griess DF, McDonald JR, Clagett OT. The proximal extension of carcinoma of the lung in the bronchial wall J Thorac Surg 1945;14:362-368.
  13. Cotton RE. The bronchial spread of lung cancer Br J Dis Chest 1959;53:142-150.[Medline]
  14. Soorae AS, Stevenson HM. Survival with residual tumor on the bronchial margin after resection for bronchogenic carcinoma J Thorac Cardiovasc Surg 1979;78:175-180.[Abstract]
  15. Kayser K, Anyanwu E, Vogt-Moykopf I. Tumor presence at the resection boundaries and lymph node metastasis in bronchial carcinoma patients Thorac Cardiovasc Surg 1993;41:308-311.[Medline]
  16. Shields TW. The fate of patients after incomplete resection of bronchial carcinoma Surg Gynecol Obstet 1974;139:569-572.[Medline]
  17. Liewald F, Hatz RA, Dienemann H, Sunder-Plassmann L. Importance of microscopic residual disease at the bronchial margin after resection for non-small cell carcinoma of the lung J Thorac Cardiovasc Surg 1992;104:408-412.[Abstract]
  18. Jeffery RM. Survival in bronchial carcinoma Ann R Coll Surg Engl 1972;51:55-59.[Medline]
  19. Kaiser LR, Fleshner P, Keller S, Martini N. Significance of extramucosal residual tumor at the bronchial resection margin Ann Thorac Surg 1989;47:265-269.[Abstract/Free Full Text]
  20. Snijder RJ, Brutel de la Rivière A, Elbers HJJ, van der Bosch JMM. Survival in resected stage I lung cancer with residual tumor at the bronchial resection margin Ann Thorac Surg 1998;65:212-216.[Abstract/Free Full Text]
  21. Ruffini E, Bongiovanni M, Cavallo A, et al. The significance of associated pre-invasive lesions in patients resected for primary neoplasms Eur J Cardiothorac Surg 2004;26:165-172.[Abstract/Free Full Text]
  22. Pasic A, Grünberg K, Mooi WJ, Paul MA, Postmus PE, Sutedja TG. The natural history of carcinoma in situ involving bronchial resection margins Chest 2005;128:1736-1741.[Medline]
  23. Massard G, Doddoli C, Gasser B, et al. Prognostic implications of a positive bronchial resection margin Eur J Cardiothoracic Surg 2000;17:557-565.[Abstract/Free Full Text]
  24. Collaud S, Bongiovanni M, Pache JC, Fioretta G, Robert JH. Survival according to the site of bronchial microscopic residual disease after lung resection for non-small cell lung cancer J Thorac Cardiovasc Surg 2009;137:622-626.[Abstract/Free Full Text]
  25. Hofmann HS, Taege C, Lautenschlager C, Neef H, Silber RE. Microscopic (R1) and macroscopic (R2) residual disease in patients with resected non small cell lung cancer Eur J Cardiothorac Surg 2002;21:606-610.[Abstract/Free Full Text]
  26. Ghiribelli C, Voltolini L, Paladini P, Luzzi L, Di Bisceglie M, Gotti G. Treatment and survival after lung resection for non-small cell lung cancer in patients with microscopic residual disease at the bronchial stump Eur J Cardiothoracic Surg 1999;16:555-559.[Abstract/Free Full Text]
  27. Lacasse Y, Bucher HC, Wong E, et al. Incomplete resection in non-small cell lung cancer: need for a new definition Ann Thorac Surg 1998;65:220-226.[Abstract/Free Full Text]
  28. Mineo TC, Ambrogi V, Pompeo E, Baldi A. Immunohistochemistry-detected microscopic tumor spread affects outcome in en-bloc resection for T3-chest wall lung cancer Eur J Cardiothorac Surg 2007;31:1120-1124.[Abstract/Free Full Text]
  29. Ratto GB, Costa R, Vassallo G, Alloisio A, Maineri P, Bruzzi P. Twelve-year experience with left atrial resection in the treatment of non-small cell lung cancer Ann Thorac Surg 2004;78:234-237.[Abstract/Free Full Text]

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