ORIGINAL ARTICLE Resection Rte nd Outcome of Pulmonry Resections for Non Smll-Cell Lung Cncer A Ntionwide Study From Icelnd Hunbogi Thorsteinsson, MD,* Asgeir Alexndersson, MD,* Gudrun N. Oskrsdottir, MD,* Rut Skuldottir, MD,* Helgi J. Isksson, MD, Steinn Jonsson, MD,* nd Toms Gudbjrtsson, MD, PhD* Bckground: The proportion of ptients with non smll-cell lung cncer (NSCLC) who undergo surgery with curtive intent is one mesure of effectiveness in treting lung cncer. To the best of our knowledge, surgicl resection rte (SRR) for whole ntion hs never been reported before. We studied the SRR nd surgicl outcome of NSCLC ptients in Icelnd during recent 15-yer period. Methods: This ws retrospective study of ll pulmonry resections performed with curtive intent for NSCLC in Icelnd from 1994 to 2008. Informtion ws retrieved from medicl records nd from the Icelndic Cncer Registry. Ptient demogrphics, postopertive tumor, node, metstsis stge, overll survivl, nd compliction rtes were compred over three 5-yer periods. Results: Of 1530 confirmed cses of NSCLC, 404 were resected, giving n SRR of 26.4%, which did not chnge significntly during the study period. Minor nd mjor compliction rtes were 37.4% nd 8.7%, respectively. Opertive mortlity rtes were 0.7% for lobectomy, 3.3% for pneumonectomy, nd 0% for lesser resection. Five-yer survivl fter ll procedures ws 40.7% nd improved from the first to the lst 5-yer period (34.8% versus 43.8%, p = 0.04). Five-yer survivl for stges I nd II together ws 46.8%, with no significnt chnge in stge distribution between periods. Five-yer survivl fter pneumonectomy ws 22.0%, which ws significntly lower thn for lobectomy (44.6%) nd lesser resection (40.7%) (p < 0.005). Unoperted ptients hd 5-yer survivl of 4.8%, s compred to 12.4% for ll the NSCLC ptients together. Conclusion: Compred with most other published studies, the SRR of NSCLC in Icelnd is high. Short-term outcome is good, with low rte of mjor complictions nd n opertive mortlity of only 1.0%. Five-yer survivl improved significntly over the study period. Key Words: NSCLC, Resection rte, Outcome, Complictions, Survivl. (J Thorc Oncol. 2012;7: 1164 1169) *Fculty of Medicine, nd Deprtment of Crdiothorcic Surgery, University of Icelnd, Reykjvik, Icelnd; Deprtments of Pthology, Pulmonology, nd Crdiothorcic Surgery, Lndspitli University Hospitl, Reykjvik, Icelnd. Disclosure: The uthors declre no conflict of interest. Address for correspondence: Toms Gudbjrtsson, MD, PhD, Deprtment of Crdiothorcic Surgery, Lndspitli University Hospitl, Reykjvik, Icelnd. E-mil: tomsgud@lndspitli.is Copyright 2012 by the Interntionl Assocition for the Study of Lung Cncer ISSN: 1556-0864/12/0707-1164 Lung cncer is the leding cuse of cncer-relted deths in the western world. 1 In Icelnd, the mortlity from lung cncer is similr to tht of brest, prostte, nd colon cncer combined, nd non smll-cell lung cncer (NSCLC) ccounts for bout 85% of lung cncer cses. 2 Although surgicl resection is still the only well-defined curtive tretment for NSCLC, it is only possible for the one third of ptients dignosed with stge I or stge II disese nd for selected cses of stge IIIA disese. 3,4,5 Surgicl resection rte (SRR) is one mesure of effectiveness in treting NSCLC, for exmple, in prticulr geogrphic loction. SRR hs vried considerbly, often rnging from 15% to 25% in Europen studies, 6 9 nd it ws 29% in study including more thn 700 hospitls in the United Sttes. 5 However, smller single-institution studies from the United Sttes hve found SRRs of up to 37%, 10 nd there hve been studies from Europe tht show SRRs s low s 10%. 6,11 13 None of the previously published studies hve found n SRR for whole ntion. The sme pplies to outcome nlysis of surgicl tretment of NSCLC. Numerous uthors hve reported short-term complictions nd long-term survivl for lobectomies, pneumonectomies, nd lesser resections seprtely, with only few of the studies nlyzing ll the different procedures together. In these studies, the combined rte of mjor complictions hs been round or over 10%, 14 16 nd opertive mortlity hs rnged from 1.5% to 7%. 5,8,14,17 19 For pneumonectomies, the figures were often double these vlues. 14 16 The im of this study ws to investigte the SRR for the whole ntion of Icelnd using centrlized dtbses in the country. Another im ws to determine surgicl outcomes for the different lung procedures tht were performed with curtive intent in NSCLC ptients in Icelnd s whole. MATERIALS AND METHODS This ws retrospective study of ll ptients in Icelnd who underwent pulmonry resection with curtive intent for NSCLC from Jnury 1, 1994 to December 31, 2008. Explortory-only thorcotomies, pllitive procedures, nd lesser resections for biopsy purposes were excluded. A centrl, computerized histology dtbse from the Deprtment of Pthology of Lndspitli University Hospitl, contining detils of ll lung histology specimens in Icelnd ws used to identify cses. To minimize the risk of cses being 1164 Journl of Thorcic Oncology Volume 7, Number 7, July 2012
Journl of Thorcic Oncology Volume 7, Number 7, July 2012 Pulmonry Resections for NSCLC, nd Resection Rte missed, we lso reviewed the dignosis nd opertion registry t Lndspitli University Hospitl, the only center performing crdiothorcic surgery in Icelnd. We obtined informtion on ll cses with histologiclly confirmed dignosis of primry NSCLC from the Icelndic Cncer Registry. 2 This registry covers ll cncer cses dignosed t hospitls nd other helthcre fcilities in Icelnd since 1955. SRR ws clculted by dividing the number of ll pulmonry resections with curtive intent for NSCLC by the number of ll histologiclly confirmed cses of NSCLC within the sme period. One hundred nd thirtythree ptients (6.6% of ll ptients with lung cncer dignosis) did not hve histologiclly confirmed dignosis, nd 306 ptients hd smll-cell crcinom. These two groups were excluded from the NSCLC group tht mde up the denomintor for the clcultion of SRR. We lso excluded ptients with crcinoid tumors (n = 38), srcoms, nd crcinom in situ. Bseline demogrphic informtion nd clinicl dt were collected from hospitl chrts nd surgicl reports using stndrdized dt sheet. Age, comorbidities, nd presenting symptoms were collected long with dt regrding the type of opertion, tumor, postopertive tumor, node, metstsis (TNM) stge, complictions, nd survivl. Ptients being considered for pulmonry resection hd been reviewed by multidisciplinry tumor bord including thorcic surgeons, pulmonologists, oncologists, rdiologists, nd pthologists. The preopertive workup vried between ptients, but usully included chest rdiogrph, computed tomogrphy (CT) scn of the chest, upper bdomen nd hed, nd lso bone scintigrphy nd spirometry. Preopertive biopsies were obtined through bronchoscopy or trnsthorcic CT-guided needle biopsy. Medistinoscopy ws performed preopertively in proportion of the cses, but positron emission tomogrphy (PET) scn hs never been vilble in Icelnd. Ptients were stged postopertively (pthologicl stge, ptnm) using both the 6th nd the 7th edition of the TNM stging system, 20 but dt is primrily reported for the 6th version. Preopertive clinicl stging (ctnm) ws not performed uniformly nd is not reported in this study. All surgicl procedures were performed in generl nesthesi with double lumen intubtion nd thorcic epidurl nesthesi. The opertions were performed by six surgeons using stndrdized techniques with intropertive lymphdenectomy of enlrged hilr or ipsilterl medistinl lymph nodes, but during the lst 5-yer period these lymph nodes were routinely removed or smpled. A posterolterl thorcotomy ws most often performed, but during the lst 5-yer period n nterolterl pproch ws used. Mjor complictions were defined s reopertion for bleeding, hert filure, cute respirtory distress syndrome, myocrdil infrction, empyem, stroke, nd bronchopleurl fistul. Minor complictions were defined s ir lekge for more thn 7 dys, pneumoni, intropertive bleeding of more thn 1 liter, tril fibrilltion/flutter, wound infection, nd recurrent lryngel nerve prlysis. Opertive mortlity ws defined s deth occurring within 30 dys of surgery. To ssess trends, the 15-yer study period ws divided into three 5-yer periods. Sttistics Microsoft Excel ws used for descriptive sttistics, nd R version 2.10.1 for survivl clcultions. Student s t test, Fisher s exct test, nd the χ 2 test were used to compre groups, nd differences were considered to be sttisticlly significnt when the p vlue ws less thn 0.05. Overll survivl (OS) ws nlyzed by the Kpln-Meier method, nd the logrnk test ws used to compre survivl between groups. All ptients were followed up with respect to survivl by using dt from the Icelndic Ntionl Popultion Registry. 21 In this wy, ptients could be ssigned dte of deth or were identified s living on July 10, 2010. Men follow-up time ws 49 months (rnge, 0 194 months). The study ws pproved by the Icelndic Ntionl Bioethics Committee nd the Dt Protection Authority. As individul ptients were not identified, individul consent ws wived. RESULTS There were 1530 histologiclly confirmed cses of NSCLC during the 15-yer period, of which 404 underwent surgery (397 ptients). The SRR ws 26.4% nd did not chnge significntly between the three 5-yer periods (28.2%, 24.3%, nd 26.8%, respectively; Tble 1). The surgicl procedures consisted of 297 lobectomies (73.5%), 60 pneumonectomies (14.9%), nd 47 lesser resections (11.6%). The men ge of ptients who underwent surgery ws 65.9 yers; those in the pneumonectomy group were 6 yers younger on verge thn those in the lesser resection group (Tble 2). Over 95% of the ptients were current or previous smokers, nd mny of them hd reduced pulmonry function. A history of coronry rtery disese nd chronic obstructive TABLE 1. Evlution of Trends From 1994 to 2008 for Ptients in Icelnd Who Underwent Surgicl Resection With Curtive Intent for NSCLC, Divided into Three 5-Yer Periods 1994 1998 (n = 124) 1999 2003 (n = 119) 2004 2008 (n = 161) All Periods Mle sex 66 (53.2) 60 (50.4) 85 (52.8) 211 (52.2) Men ge 64.4 65.4 67.1 65.8 Age > 69 yers 46 (37.1) 48 (40.3) 74 (46.0) 168 (41.6) Surgicl resection 28.2 24.3 26.8 26.4 rte (SRR), % Adenocrcinom 67 (54.0) 64 (53.8) 103 (64.0) 234 (57.4) histology Incidentl 40 (32.8) 38 (31.9) 61 (37.9) 139 (34.6) dignosis Medistinoscopy 11 (8.9) 21 (17.6) 25 (15.5) 57 (14.1) performed Stge I or II 98 (79.0) 94 (79.0) 126 (7.83) 318 (78.7) disese Pneumonectomies 16 (12.9) 18 (15.1) 26 (16.1) 60 (14.9) 5-yer survivl, % 34.8 40.6 43.8 40.7 The numbers of ptients re given with percentges in prentheses, except for ge, surgicl resection rte, nd survivl, where men nd percentge re given. Sttisticlly significnt difference between groups (p < 0.05). NSCLC, non smll-cell lung cncer. Copyright 2012 by the Interntionl Assocition for the Study of Lung Cncer 1165
Thorsteinsson et l. Journl of Thorcic Oncology Volume 7, Number 7, July 2012 TABLE 2. Ptient Demogrphics nd Comorbidities in Ptients in Icelnd, Who Underwent Surgicl Resection With Curtive Intent for NSCLC, 1994 to 2008 Lobectomy (n = 297) Pneumonectomy (n = 60) Lesser Resections (n = 47) All Procedures Mle sex 148 (49.9) 42 (70.0) 21 (44.7) 211 (52.2) Age, yers (rnge) 65.9 (37 89) 62.7 (45 83) 69.1 (43 84) 65.8 (37 89) History of smoking 285 (96.0) 59 (98.3) 46 (97.9) 390 (96.5) COPD 73 (24.7) 14 (23.3) 19 (40.4) 106 (26.3) FEV1 < 75% predicted 83 (27.9) 20 (33.3) 20 (42.6) 123 (30.5) Coronry rtery disese 72 (24.2) 12 (20.0) 26 (55.3) 110 (27.2) ASA score, men 2.6 2.6 2.6 2.6 The numbers of ptients re given with percentges in prentheses, except for ge nd ASA score where mens re given. Sttisticlly significnt difference between groups (p < 0.05). NSCLC, non smll-cell lung cncer; COPD, chronic obstructive pulmonry disese; FEV1, forced expirtory volume in 1 second; ASA, Americn Society of Anesthesiologists. pulmonry disese ws significntly more common in ptients who underwent lesser resection thn in ptients who underwent pneumonectomy or lobectomy. A forced expirtory volume of less thn 75% of the predicted vlue in 1 second ws lso identified in more ptients who underwent lesser resection (42.6% versus 28.9% for the other ptients, p = 0.06; Tble 2). Adenocrcinom ws the most common histologicl type of lung cncer (57.4%), wheres squmous-cell histology ccounted for 31.7% (Tble 3). Squmous-cell crcinom ws more frequent in those who underwent pneumonectomy thn in the other ptients. As shown in Tble 3, lmost 87% of the ptients hd stge I, stge II, or stge IIIA disese, but 13.9% hd stge IIIB or IV disese in postopertive stging. The proportion of stge I cses ws highest in the ptients who underwent lesser resection (78.7%). In Tble 4 the stge distribution using the 7th edition of the TNM system is lso given. The stge distribution did not chnge significntly between periods (Tble 1). A medistinoscopy ws performed preopertively in 20 of the pneumonectomies (33.3%), in 36 of the lobectomies (12.1%), nd in one of the lesser resections (2.1%). Almost 9% of the ptients hd mjor complictions, of which reopertion for bleeding (n = 9), reopertion for empyem nd/or bronchopleurl fistul (n = 7), hert filure (n = 7), nd myocrdil infrction (n = 6) were the most common (Tble 5). The rte of mjor complictions ws significntly higher for the ptients who underwent pneumonectomy (18.3%) thn for those who underwent lobectomy (7.1%) nd lesser resection (6.4%) (p = 0.01; Tble 5). Two ptients died within 30 dys of lobectomy nd two others died fter pneumonectomy, but there ws no opertive mortlity fter lesser resection. Opertive mortlity for the whole group ws therefore 1.0%. Five-yer OS for the whole group ws 40.7%. It ws significntly higher for the lst 5-yer period thn for the first (43.8% versus 34.8%; log-rnk test, p = 0.039) (Tble 1). Figure 1 shows OS for the different procedures. Survivl t 5 yers ws 44.6% fter lobectomy, 40.7% fter lesser resection, TABLE 3. Tumor Histology, Disese Stge (ptnm), nd Other Pthologicl Dt for Ptients in Icelnd, Who Underwent Surgicl Resections (Lobectomy, Pneumonectomy, nd Lesser Resections) with Curtive Intent for NSCLC, 1994 to 2008 Lobectomy (n = 297) Pneumonectomy (n = 60) Lesser Resections (n = 47) All Procedures Tumor histology Adenocrcinom 179 (60.2) 22 (36.7) 31 (66.0) 138 (57.4) Squmous-cell 85 (28.6) 32 (53.3) 11 (23.4) 128 (31.7) Lrge-cell 19 (6.4) 3 (5.0) 1 (2.1) 23 (5.7) Other (including denosqumous) 13 (4.3) 3 (5.0) 4 (8.5) 20 (5.0) Disese stge (ptnm) I 179 (60.2) 8 (13.3) 37 (78.7) 224 (55.4) II 59 (19.9) 27 (45.0) 8 (17.0) 94 (23.3) IIIA 19 (6.4) 9 (15) 2 (4.3) 30 (7.4) IIIB 22 (7.4) 13 (21.7) 0 35 (8.7) IV 18 (6.1) 3 (5.0) 0 21 (5.2) Men size of tumor, mm (rnge) 39 (4 190) 57 (20 150) 23 (8 50) 40 (4 190) Positive surgicl mrgins 27 (9.1) 7 (11.7) 9 (18.8) 43 (10.6) The numbers of ptients re given with percentges in prentheses, except for tumor size where mens with rnge re given. Sttisticlly significnt difference between groups (p < 0.05). TNM, tumor, node, metstsis; NSCLC, non smll-cell lung cncer. 1166 Copyright 2012 by the Interntionl Assocition for the Study of Lung Cncer
Journl of Thorcic Oncology Volume 7, Number 7, July 2012 Pulmonry Resections for NSCLC, nd Resection Rte TABLE 4. Overll 5-Yer Survivl According to Both the 6th nd 7th Edition of the TNM Stging System for Ptients in Icelnd With NSCLC Who Underwent Surgicl Resection With Curtive Intent, 1994 to 2008 TNM Stge 6th Edition (n) Survivl t 5 Yers (%) 7th Edition (n) Survivl t 5 Yers (%) I 224 55.3 194 58.1 II 94 26.6 128 29.4 IIIA 30 19.9 61 22.1 IIIB 35 23.8 3 NA IV 21 7.1 18 5.4 I + II 318 46.8 322 46.7 III + IV 86 18.4 82 17.8 Only three ptients, clcultions therefore not vilble. NA, not vilble. nd significntly lower (22.0%) fter pneumonectomy (p = 0.006). The NSCLC ptients who did not undergo surgery hd much less fvorble survivl: only 4.8% fter 5 yers. Survivl for ll NSCLC ptients together ws 12.4% t 5 yers, but 46.8% for stges I nd II together for the operted ptients. Survivl for the different stges is shown in Tble 4 nd Figure 2. DISCUSSION Our results show tht the SRR for NSCLC in Icelnd (t 26.4%) is higher thn in other Europen studies, where SRR hs usully been reported to be in the 15% to 25% rnge. 6 9 To the best of our knowledge, this is the first report of SRR for whole ntion. Short-term outcome for ll procedures ws excellent, with low rtes of mjor complictions nd n opertive mortlity of only 1.0%; other studies hve found figures between 1.5% nd 7%. 5,8,14,17 19 The rte of mjor complictions ws 8.7%, which is low compred to other studies. However, comprisons between studies cn be difficult becuse of the different criteri used. In the study by Myrdl et l. 14 the rte of mjor complictions ws 8.8%, nd it ws 12.4% in the study by Yno et l. 15 In nother study, the mjor compliction rte ws 13%, but the uthors definition of mjor complictions ws wider thn tht in the present study. 16 Five-yer survivl in this study ws 40.7% for the whole study period nd it improved from 34.8% during the first 5-yer period to 43.8% for the lst 5-yer period (p = 0.04). Survivl figures from other studies hve rnged from 30% to 60% t 5 yers, 10,22 24 nd from round 50% to 60% for ptients with stge I nd II disese, which re somewht higher thn observed for stge I nd II ptients in our study, or 47%. 20 Few studies evluting surgicl outcomes of NSCLC hve included ll three types of opertions. In this study, survivl fter lesser resection ws similr to tht fter lobectomy, even though higher proportion of ptients in the lesser resection group hd underlying crdiopulmonry disese. There ws, however, higher proportion of ptients with stge I disese in the lesser-resection group. The low compliction rte nd low mortlity rte in the lesser-resection group rises the question of whether some of these ptients could hve TABLE 5. Minor nd Mjor Complictions in Ptients in Icelnd Who Underwent Different Lung Opertions With Curtive Intent for NSCLC, 1994 to 2008 Lobectomy (n = 297) Pneumonectomy (n = 60) Lesser Resections (n = 47) All Procedures Minor complictions 105 (35.4) 30 (50.0) 16 (34.0) 151 (37.4) Intropertive bleeding 24 (8.1) 20 (33.3) 0 (0) 44 (10.9) > 1 l Atril fibrilltion/flutter 18 (6.1) 15 (25.0) 1 (2.1) 34 (8.4) Recurrent lryngel 5 (1.7) 2 (3.3) 0 (0) 7 (1.7) nerve prlysis Air lekge for > 7 dys 63 (21.2) 1 (1.7) 6 (12.8) 70 (17.3) Pneumoni 16 (5.4) 3 (5.0) 7 (14.9) 26 (6.4) Wound infection 5 (1.7) 1 (1.7) 2 (4.3) 8 (2.0) Mjor complictions 21 (7.1) 11 (18.3) 3 (6.4) 35 (8.7) ARDS 6 (2.0) 3 (5.0) 0 9 (2.2) Reopertion for 6 (2.0) 3 (5.0) 0 9 (2.2) bleeding Reopertion for 3 (1.0) 4 (6.7) 0 7 (1.7) empyem nd/or BPF Hert filure 6 (2.0) 0 1 (2.1) 7 (1.7) Myocrdil infrction 4 (1.3) 1 (1.7) 1 (2.1) 6 (1.5) Empyem 3 (1.0) 3 (5.0) 0 6 (1.5) Bronchopleurl fistul 1 (0.3) 1 (1.7) 0 2 (0.5) Stroke 0 0 1 (2.1) 1 (0.2) A ptient could hve more thn one compliction. The numbers of ptients re given with percentges in prentheses. Sttisticlly significnt difference between groups (p < 0.05). NSCLC, non smll-cell lung cncer; ARDS, cute respirtory distress syndrome; BPF, bronchopleurl fistul. Copyright 2012 by the Interntionl Assocition for the Study of Lung Cncer 1167
Thorsteinsson et l. Journl of Thorcic Oncology Volume 7, Number 7, July 2012 FIGURE. 1. Kpln-Meier grph showing overll survivl of ptients with NSCLC who underwent surgicl resection (lobectomy, pneumonectomy, or lesser resections) with curtive intent in Icelnd from 1994 to 2008. Ptients who did not undergo surgery re lso shown. NSCLC, non smll-cell lung cncer. tolerted lobectomy. Alterntively, this could lso be n rgument for greter use of lesser resections in ptients with smll tumors. This question is being ctively studied, s there is growing evidence tht lesser resections re resonble pproch for smll peripherl tumors (of < 2 cm) nd lso for smll ground-glss opcity lesions detected by CT imging. 25 As expected, survivl fter pneumonectomy ws significntly lower thn fter lobectomy nd lesser resection. Our result of 22% 5-yer survivl fter pneumonectomy seems disproportiontely low when compred to the results of other studies tht hve shown rtes from 27% to 40%. 26 29 The reson for the low survivl fter pneumonectomy is open to debte, but understging becuse of low rte of medistinoscopies my hve hd role. Tumors requiring pneumonectomy re often lrge nd centrlly locted, nd spred more often to the medistinl lymph nodes, mking medistinoscopy even more importnt in the workup of these ptients. 30 The use of PET scns, which ws not vilble for this ptient popultion, is lso known to improve preopertive stging nd to prevent unnecessry surgery. As shown in Tble 1, it is unlikely tht stge distribution explins improved survivl, s it did not chnge significntly during the study period. A number of dvnces hve been mde in the preopertive evlution nd stging of ptients with NSCLC in recent yers. Improvements in imging techniques nd incresed use of medistinoscopy my hve resulted in more ptients being excluded from surgicl resection becuse of dvnced disese. This could hve contributed to the fct tht survivl improved during the lst 5-yer period of this study. Improvements in surgicl techniques, with increses in the number of cses operted on per surgeon, re lso known to ply role. 24 Finlly, more frequent use of djuvnt chemotherpy for stge II disese during the lst period might lso hve contributed to improved survivl. 31 This is retrospective study with the potentil bis tht it cn introduce, problems like lck of complete preopertive stge nd documenttion of complictions. Furthermore, PET scn ws not vilble in Icelnd for stging, nd medistinoscopy ws used routinely for medistinl stging during the lst 5 yers of the study. The strength of this study is tht our cohort consisted of ptients from whole popultion, ll of whom were operted on in single center. The results were therefore less likely to be ffected by tertiry referrl. We hve reported resection rte, rtes of complictions, nd survivl rtes for ll ptients who underwent surgery with curtive intent for NSCLC in the Icelndic popultion during 15-yer period. In our opinion, these dt should be reported together in context to help evlute the outcome of surgicl cre for ptients with NSCLC. Furthermore, we hve reported survivl of ptients with NSCLC who were not operted on, which is importnt for comprison. FIGURE. 2. Kpln-Meier grph showing overll survivl of ptients with NSCLC, both for stges I nd II, nd III nd IV together, who underwent surgicl resection with curtive intent in Icelnd from 1994 to 2008. NSCLC, non smll-cell lung cncer. REFERENCES 1. Prkin DM, Bry F, Ferly J, Pisni P. Globl cncer sttistics, 2002. CA Cncer J Clin 2005;55:74 108. 2. Icelndic Cncer Society. About ICR. Avilble t: http://www. krbbmeinsskr.is/indexen.jsp?id=b (Accessed July 3, 2011). 3. Scott WJ, Howington J, Feigenberg S, Movss B, Pisters K; Americn College of Chest Physicins. Tretment of non-smll cell lung cncer stge I nd stge II: ACCP evidence-bsed clinicl prctice guidelines (2 nd edition). Chest 2007;132(3 Suppl):234S 242S. 4. Robinson LA, Ruckdeschel JC, Wgner H Jr, Stevens CW; Americn College of Chest Physicins. Tretment of non-smll cell lung cncerstge IIIA: ACCP evidence-bsed clinicl prctice guidelines (2 nd edition). Chest 2007;132(3 Suppl):243S 265S. 5. Little AG, Rusch VW, Bonner JA, et l. Ptterns of surgicl cre of lung cncer ptients. Ann Thorc Surg 2005;80:2051 2056; discussion 2056. 6. Lroche C, Wells F, Coulden R, et l. Improving surgicl resection rte in lung cncer. Thorx 1998;53:445 449. 7. Crtmn ML, Htfield AC, Muers MF, Peke MD, Hwrd RA, Formn D; Yorkshire Cncer Mngement Study Group, Northern nd Yorkshire 1168 Copyright 2012 by the Interntionl Assocition for the Study of Lung Cncer
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