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umor Location Is Not an Independent Prognosticactor in Early Stage Non-Small Cell Lung Cancerarun Puri, MD, Nitin Garg, MD, Erin E. Engelhardt, BS, Daniel Kreisel, MD, PhD,raves D. Crabtree, MD, Bryan F. Meyers, MD, MPH, G. Alexander Patterson, MD, andlexander Sasha Krupnick, MD

epartment of Surgery, Washington University in St. Louis, St. Louis, Missouri, and Department of Surgery, Creighton

niversity, Omaha, Nebraska

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Background. Conventional thoracic surgical teachinguggests a worse outcome for lower lobe lung cancers. Its unclear whether this is due to stage migration orhether lobar location is an independent negative prog-ostic factor.Methods. We performed a retrospective review of our

nstitutional database of patients undergoing resectionor pathologic stage I or stage II lung cancer between Jan000 and December 2006. Survival analysis was used toompare outcomes in various groups using the log-rankest. Logistic regression analysis was used to compare therimary dependent variables; age, size, and location of

umor (both laterality and lobe), histology (adenocarci-oma, squamous, large cell, or neuroendocrine and oth-rs) and type of resection (wedge, lobectomy or segmen-ectomy, and pneumonectomy).

Results. A total of 841 patients met the inclusionriteria. The mean age of patients was 64.9 years, mean

umor size 3.3 cm, and, 144 patients had N1 disease. The

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urgery, Washington University in St Louis, 660 S Euclid Ave, St Louis,O 63110; e-mail: krupnicka@wudosis.wustl.edu.

2010 by The Society of Thoracic Surgeonsublished by Elsevier Inc

hree-year and five-year survivals for stage I tumors were46 of 478 (72.4%) and 277 of 497 (55.7%), respectively.here was no difference in survival based upon lobar

ocation. The three-year and five-year survivals for stageI tumors were 81 of 175 (46.3%) and 39 of 150 (26%),espectively, and lobar location did not influence sur-ival. Logistic regression analysis showed that for stage Iumors increasing age and having undergone a pneumo-ectomy were associated with worse survival, and fortage II tumors increasing age and adenocarcinoma his-ology were associated with worse survival.

Conclusions. Tumor location within the lung does notredict survival in pathologic stage I/II non–small cell

ung carcinoma. Increasing age, adenocarcinoma histol-gy, and pneumonectomy as the resection may lead toorse long-term survival.

(Ann Thorac Surg 2010;89:1053–9)

© 2010 by The Society of Thoracic Surgeons

espite current-day ideal treatment, the five-yearsurvival in patients with stage I non-small cell lung

ancer (NSCLC) is only 60% [1]. This highlights themportance of looking for prognostic indicators that mayichotomize early stage NSCLC patients into differentisk categories. Molecular markers and gene expressionrofiling have been looked at as prognostic indicatorsnd may eventually be important in selecting patients forhemotherapy or biologic therapy, but to date the deci-ion for adjuvant therapy has been mostly made by stage2]. Thus, the identification of other clinicopathologiceatures that may lead to worse prognosis independent oftage may have clinical utility in offering postoperativedjuvant therapy to a subgroup of patients.Conventional thoracic surgical teaching has suggestedworse outcome for lower lobe lesions [3–6]. The reason

or this discrepancy in survival has, however, remainedontroversial. Some investigators have suggested thaturvival is statistically worse for stage I non-upper lobeesions, irrespective of other prognostic factors [4]. Other

ccepted for publication Jan 4, 2010.

ddress correspondence to Dr Krupnick, Division of Cardiothoracic

nvestigators have shown non-upper lobe tumor locationo be an adverse prognostic variable in pathologic stageII lung cancer also [5, 7, 8]. Such differences in pathologicehavior could conceptually be attributed to differences

n ventilation and perfusion in the different zones of theung, leading to asymmetric distribution of aerosolizedarcinogens, or other factors such as heterogeneity inngiogenesis between different zones of the lung [9, 10].An alternative school of thought suggests that theorse prognosis of lower lobe tumors might be due to aigher rate of lymphatic metastases and unrecognizedetastatic disease leading to understaging. In fact, a

ve-year prospective study found lower lobe tumor loca-ion to be a significant factor in upstaging at the time ofurgery [6]. One can thus argue that large multiinstitu-ional studies which do not control for surgical factorsuch as degree of intraoperative lymph node dissectionight be confounded by such understaging [4]. As it has

een our uniform institutional practice to perform medi-stinoscopy, intraoperative lymph node dissection, orggressive sampling at the time of resection, we decidedo investigate the role of lobar tumor distribution onurvival in early-stage lung cancer by a single institution

eview study. The purpose of this study was to examine

0003-4975/10/$36.00doi:10.1016/j.athoracsur.2010.01.020

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1054 PURI ET AL Ann Thorac SurgTUMOR LOCATION AS A PROGNOSTIC FACTOR IN LUNG CANCER 2010;89:1053–9

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he influence of lobar location of tumor as an indepen-ent prognostic factor for survival in stage I and IISCLC. We hypothesize that for early-stage lung cancer,

obar location is not an independent predictor forurvival.

aterial and Methods

e performed a retrospective review of our institutionalatabase of patients undergoing surgical procedures for

ung cancer between January 2000 and December 2006.f these, patients who met the following criteria were

elected: underwent resection of tumor; completed twoears of follow-up or died; and had pathologically stage Ir II cancers. All epidemiologic, clinical, pathologic, andollow-up data were abstracted from the institutionalatabase or records. Individual charts were reviewedhere information was incomplete. All patient recordshere institutional follow-up was not available were

onfirmed with the Social Security Death Index.Patients lost to follow-up prior to a three-year periodere not included in the statistical analysis (censoredbservations). The last date of follow-up was May 31,008 (date of data collection from national Social Securityeath Index database). Patients with pathologic stage I

nd II were analyzed separately. Primary dependentariables analyzed were age, size and location of theumor (both laterality and lobe), histology (adenocarci-oma, squamous, large cell or neuroendocrine, and oth-rs), and type of resection (wedge, lobectomy or segmen-ectomy, and pneumonectomy).

The surgical procedures performed included wedgeesection, segmentectomy, lobectomy, and pneumonec-omy. The operations were performed through a thora-otomy or video-assisted thoracoscopy by a group of sixhoracic surgeons.

All patients with carcinoma in situ, bilateral or multi-entric tumors, and tumors located at fissure incorporat-ng more than one lobe were excluded from analysis.ata thus abstracted were entered into an Excel (Mi-

rosoft, Redmond, WA) spreadsheet and analyzed using

able 1. Basic Demographic, Histology, and Operative Datay Pathologic Stage

ariables Stage I Stage II

umber 621 220ean age (years) 65 64.8istologyAdenocarcinoma 335 (53.9%) 80 (36.4%)Squamous 165 (26.5%) 101 (45.9%)Large cell/neuroendocrine 54 (8.7%) 16 (4.5%)Others 67 (10.4%) 23 (10.5%)

ype of resectionWedge 57 (9.2%) 6 (2.7%)Segmentectomy 26 (4.2%) 5 (2.3%)Lobectomy 523 (84.2%) 177 (80.5%)

Pneumonectomy 15 (2.4%) 32 (14.5%) L

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tata (StataCorp LP, College Station, TX). Survival anal-sis was used to compare outcomes (death) in variousroups using the log-rank test. The Cox proportionalazards model was used to test the effect of independentariables. In the absence of proportional hazards onisual inspection of Kaplan-Meier graphs, logistic regres-ion was used to compare groups for three-year andve-year survival. A p value of less than 0.05 was consid-red significant.

esults

total of 841 patients met the inclusion criteria. Theean age of patients was 64.9 years. The mean tumor sizeas 3.3 cm and 144 patients had N1 disease. The median

ength of hospital stay was six days. The demographicata and tumor and operative characteristics are summa-ized in Tables 1 and 2. The data showing intraoperativeediastinal lymph node assessment are summarized in

able 3.The majority of tumors (540 of 841) were in the upper

obes and right-sided lesions were more common thaneft-sided lesions (494 vs 347). Of the 621 patients withtage I NSCLC 387 were located in the upper lobes, 200 inhe lower, and 34 in the middle lobes, respectively. Of the20 stage II cancers 143 were in the upper, 67 were in theower, and 10 were in the middle lobes.

For pathologic stage I tumors, clinical and radiographiccomputed tomographic scan) staging inaccurately sug-ested nodal disease in 55 of 621 giving a false positive

able 2. Basic Demographic, Histology, and Operative Datay Lobar Location

ariables Upper Lobe Lower Lobe p Value

ge (mean � SD) 64.7 � 10.9 66.1 � 11.68 0.09tage I 387 (73%) 200 (75%) 0.57tage II 143 (27%) 67 (25%)ize � 2 cm 356 (68%) 202 (77%) 0.02denoca 282 (53%) 100 (37%)quamous 157 (30%) 115 (43%) 0.04arge cell 24 (5%) 21 (8%)edge 40 (8%) 26 (10%)

obectomy 468 (88%) 218 (82%) 0.02neumonectomy 22 (4%) 23 (8%)

able 3. Percentage of Patients Undergoing Intraoperativeediastinal Lymph Node Assessment at Resection for Stage

/II Non-Small Cell Lung Cancer

obeStations2 and 4 Station 7

Stations8 and 9

Station5 or 6

UL 80% 75% 14% —LL 72% 87% 18% —UL 44% 59% 28% 67%LL 60% 79% 66% 23%

LL � left lower lobe; LUL � left upper lobe; RLL � right lowerobe; RUL � right upper lobe.

1055Ann Thorac Surg PURI ET AL2010;89:1053–9 TUMOR LOCATION AS A PROGNOSTIC FACTOR IN LUNG CANCER

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Fig 1. Kaplan-Meier survival estimates by lobefor stage I right-sided tumors (p � 0.71). (——lobe � upper lobe; --- lobe � middle lobe; – – –lobe � lower lobe.)

Fig 2. Kaplan-Meier survival estimates bylobe for stage I left-sided tumors (p � 0.9).(—lobe � upper lobe; – – – lobe � lower lobe.)

Fig 3. Kaplan-Meier survival estimates by lat-erality; comparison of stage I upper lobe tu-mors (p � 0.54). (— side � right; – – –side � left.)

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ig 4. Kaplan-Meier survival estimates by lat-rality; comparison of stage I lower lobe tumorsp � 0.73). (— side � right; – – –ide � left.)

ig 5. Kaplan-Meier survival estimates by lat-rality; comparison of lower lobe stage II tu-ors (p � 0.6). (— side � right; – – –

ide � left.)

ig 6. Kaplan-Meier survival estimates by lat-rality; comparison of stage II upper lobe tu-ors (p � 0.45). (— side � right; – – –

ide � left.)

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ate of 8.9%. Similarly, in patients with stage II tumors,linical and radiographic staging had a false positive ratef 10% (22 of 220) in predicting mediastinal lymph node

nvolvement (N2 disease).Four hundred ninety-seven patients who had died or

ompleted at least a five-year survival period were eval-ated for the regression analysis. The three-year andve-year survivals for stage I tumors were 346 of 478

72.4%) and 181 of 347 (53%), respectively. Figuresthrough 4 represent the Kaplan-Meier survival curves

or patients with stage I tumors. For stage I tumors, thereere no statistically significant differences in survivaletween upper and non-upper lobe tumors or betweenight-sided and left-sided tumors.

The three-year and five-year survival for stage II tu-ors were 81 of 175 (46.3%) and 39 of 150 (26%), respec-

ively. For stage II tumors, the patients with lower lobeumors had similar outcomes irrespective of lateralityFig 5). Similarly, patients with right upper lobe and leftpper lobe tumors had comparable long-term survival

Fig 6). As with stage I tumors, upper lobe versus non-pper lobe location had no impact on survival (Figs 7; 8).For logistic regression analysis, to identify risk factors

or death, patient age, tumor size and histology, type ofesection, laterality, and location of tumor were consid-

red as variables. Only patients with five years of fol-ow-up were evaluated for this analysis. For stage Iumors increasing age was associated with worse survivalhile having undergone a pneumonectomy showed a

rend toward worse survival (Table 4). For patients withtage II tumors, increasing age was associated with worseurvival and adenocarcinoma histology showed a trendoward increased odds of mortality over a five-yearollow-up (Table 4).

omment

n this report we identified that there is no difference inurvival based upon lobar location in patients who un-erwent resection for pathologic stage I or II lung cancer.dditionally, increasing age at diagnosis is consistentlyssociated with increased mortality.Several reports have suggested that lower lobe location

s associated with worse long-term survival in lungancer [4, 5, 8, 11]. Ou and colleagues [4] demonstratedhat tumors located in the non-upper lobes (right middleobe, right lower lobe, left lower lobe) independentlyarried an increased risk of mortality in patients withtage IB NSCLC compared with tumors located in thepper lobes. Similarly, Iwasaki and colleagues [11], in a

Fig 7. Kaplan-Meier survival estimates by lobefor stage II right-sided tumors (p � 0.325). (—lobe � upper lobe; – – – lobe � non-upperlobe.)

Fig 8. Kaplan-Meier survival estimates by lobefor stage II left-sided tumors (p � 0.51). (—lobe � upper lobe; – – – lobe � lower lobe.)

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ultivariate analysis of patients undergoing surgery for2 tumors, reported that patients with a left lower lobe

umor location had significantly worse survival outcomesompared with patients who had tumors with other lobarocations. Ichinose and colleagues [5] also reported sim-lar differences in survival based upon lobar location inatients with resected stage IIIA NSCLC. In their series,atients with upper lobe tumors had a better long-termurvival compared with patients with middle lobe orower lobe tumors.

Stage migration may be the most important factor inhe findings of these studies, some of which [4, 8] con-idered the clinical stage in their analysis. Tumors lo-ated in upper lobes are less likely to metastasize toubcarinal lymph nodes while tumors in the lower lobesend to involve paraesophageal and inferior pulmonaryigament lymph nodes [12, 13], which are detected only atperation. Rocha and colleagues [6] found that havinghe primary tumor in a lower lobe location was the onlytatistically significant factor associated with upstagingnd other factors like patient age, smoking history,eight loss, tumor size, and tumor histology were all

ound not to be associated with upstaging. Our data,hich demonstrate no difference in survival based upon

obar location in pathologic stage I/II lung cancer, sup-ort the conclusions of Rocha and colleagues, and sug-est that stage migration and not tumor location isesponsible for differences in survival between patientsith upper and non-upper lobe tumors.Our series showed that 15 of 621 (2.5%) patients un-

erwent pneumonectomy for stage I lung cancer. Factorshat lead to what appears to be overly aggressiveurgery for early-stage disease are the following: cen-rally located tumors that are difficult to assess clini-ally; lobar atelectasis; and presence of enlarged hilarymph nodes that are inflammatory on pathologicnalysis. These 15 patients had worse long-term sur-ival compared with patients treated by lesser resec-ions, consistent with published literature showingecreased stage-specific survival in patients treated byneumonectomy [14, 15].Increasing age is consistently associated with worse

ong-term survival in our series as well as others [4, 16].his can be explained by the higher probability of dying

able 4. Results of Logistic Regression Analysis to Identify Ri

Stage I

ariables Odds Ratio of Death 95%

ge (every year increase) 1.05 1.03eft vs right 0.94 0.59ower vs upper lobe 0.87 0.54ize � 2 cm vs � 2 cm 1.37 0.83denocarcinoma vs squamous 0.95 0.56edge vs lobectomy 1.9 0.87

neumonectomy vs lobectomy 5.18 0.91

I � confidence interval.

rom unrelated causes, possible preoperative and intra-

perative understaging, and probability of a lesser oper-tion like a wedge resection than a standard lobectomy.

e also found a trend toward worse outcomes in patientsith stage II adenocarcinoma versus squamous carci-oma. Similar conclusions have been published byoldvay and colleagues [17], who found in a series of 227

atients with a surgically resected NSCLC that patientsith squamous cell carcinoma experienced fewer re-

apses than those with adenocarcinoma. Other authorsave documented similar differences in outcome foratients with squamous histology [18, 19], suggesting thathile tumor location in and of itself does not alter patient

urvival but tumor histology might. Thus, unlike thetudy by Ou and colleagues in a large multicenter state-ased trial [4], we found that tumor location within the

ung does not independently predict survival in patho-ogic stage I/II NSCLC.

e would like to thank Yvette Carter and Jennifer Zoole forssistance with the database analysis.

eferences

1. Fry WA, Philips JL, Menck HR. Ten-year survey of lungcancer treatment and survival in hospitals in the UnitedStates: a national cancer data base report. Cancer 1999;86:1867–6.

2. Schettino C, Bareschino MA, Maione P, Rossi A, Ciardiello F,Gridelli C. The potential role of pharmacogenomic andgenomic in the adjuvant treatment of early stage non smallcell lung cancer. Curr Genomics. 2008;9:252–62.

3. Kaiser LR, Jamieson GG, eds. Operative thoracic surgery,5th ed. New York, NY: Edward Arnold; 2006.

4. Ou SH, Zell JA, Ziogas A, Anton-Culver H. Prognosticfactors for survival of stage I nonsmall cell lung cancerpatients: a population-based analysis of 19,702 stage I pa-tients in the California Cancer Registry from 1989 to2003.Cancer 2007;110:1532–41.

5. Ichinose Y, Kato H, Koike T, et al. Completely resected stageIIIA non-small cell lung cancer: the significance of primarytumor location and N2 station. J Thorac Cardiovasc Surg2001;122:803–8.

6. Rocha AT, McCormack M, Montana G, Schreiber G. Asso-ciation between lower lobe location and upstaging for early-stage non-small cell lung cancer. Chest 2004;125:1424–30.

7. Inoue M, Sawabata N, Takeda S, Ohta M, Ohno Y, Maeda H.Results of surgical intervention for p-stage IIIA (N2) non-

ctors for Mortality in Stage I/II Lung Cancer

Stage II

p Value Odds Ratio of Death 95% CI p Value

�0.001 1.06 1.01–1.10 0.0060.78 0.85 0.36–2.00 0.710.57 1.5 0.59–3.9 0.390.22 0.7 0.16–2.99 0.630.86 2.43 0.96–6.14 0.060.11 0.61 0.04–8.71 0.710.06 1.26 0.41–3.88 0.68

sk Fa

CI

–1.08–1.48–1.41–2.27–1.63–4.26–29.5

small cell lung cancer: acceptable prognosis predicted bycomplete resection in patients with single N2 disease with

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primary tumor in the upper lobe. J Thorac Cardiovasc Surg2004;127:1100–6.

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1. Iwasaki A, Shirakusa T, Enatsu S, et al. Is T2 non-small celllung cancer located in left lower lobe appropriate to up-stage? Interact Cardiovasc Thorac Surg 2005;4:126–9.

2. Kotoulas CS, Foroulis CN, Kostikas K, et al. Involvement oflymphatic metastasis spread in non-small cell lung canceraccording to the primary cancer location. Lung Cancer2004;44:183–91.

3. Cerfolio RJ, Bryant AS. Distribution and likelihood of lymphnode metastasis based on the lobar location of nonsmall-celllung cancer. Ann Thorac Surg 2006;81:1969–73.

4. Martin-Ucar AE, Chaudhuri N, Edwards JG, Waller DA. Can

equirements for Maintenance

pplication has been approved. Taking SESATS in lieu of

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2010 by The Society of Thoracic Surgeonsublished by Elsevier Inc

An audit of parenchymal sparing lung surgery. EurJ Cardiothorac Surg 2002;21:601–5.

5. Ludwig C, Stoelben E, Olschewski M, Hasse J. Comparisonof morbidity, 30-day mortality, and long-term survival afterpneumonectomy and sleeve lobectomy for non-small celllung carcinoma. Ann Thorac Surg 2005;79:968–73.

6. Mery CM, Pappas AN, Bueno R, et al. Similar long-termsurvival of elderly patients with non-small cell lung cancertreated with lobectomy or wedge resection within the sur-veillance, epidemiology, and end results database. Chest2005;128:237–45.

7. Moldvay J, Scheid P, Wild P, et al. Predictive survivalmarkers in patients with surgically resected non-small celllung carcinoma. Clin Cancer Res 2000;6:1125–34.

8. Ichinose Y, Yano T, Asoah H, Yokoyama H, Yoshino I,Katsuda Y. Prognostic factors obtained by a pathologicexamination in completely resected non-small cell lungcancer: an analysis in each pathologic stage. J Thorac Car-diovasc Surg 1995;110:601–5.

9. Mountain CF, Lukeman JM, Hammar SP, et al. Lung cancerclassification: the relationship of disease extent and cell typeto survival in a clinical trails population. J Surg Oncol

pneumonectomy for non-small cell lung cancer be avoided? 1987;35:147–56.

of Certification in 2010

iplomates of the American Board of Thoracic SurgeryABTS) who plan to participate in the 2010 Maintenancef Certification (MOC) process as Certified-Active mustold an unrestricted medical license in the locale of theirractice and privileges in a hospital accredited by the

CAHO (or other organization recognized by the ABTS).n addition, a valid ABTS certificate is an absolute re-uirement for entrance into the Maintenance of Certifi-ation process. If your certificate has expired, the onlyathway for renewal of a certificate is to take and pass theart I (written) and the Part II (oral) certifying examina-

ions.The CME requirements are 90 Category I credits

arned since January 1, 2008. At least half of these CMEours need to be in the broad area of thoracic surgery.ategory II credits are not allowed. Interested individu-ls should refer to the Board’s website for a completeescription of acceptable CME credits.Diplomates who hold certificates that end in 2010 or

011 will be required to complete all sections of SESATSfter their applications have been approved. It is notecessary for Diplomates to purchase SESATS individu-lly because it will be sent to them after their applicationas been approved.Diplomates who hold certificates that end in 2012 will

e required to take and pass a secured exam after their

he secured exam is not an option. The secured exam wille given in an electronic format at testing centers located

hroughout the United States.Diplomates who wish to maintain a Certified-Active

tatus will be required to submit a summary of cases andill be required to participate in an outcomes database.or more details about this requirement, please visit theoard’s website at www.abts.org.Diplomates may apply for Maintenance of Certification

n the year their certificate expires, or if they wish to doo, they may apply up to two years before it expires.owever, the new certificate will be dated 10 years from

he date of expiration of their original certificate or mostecent recertification certificate. In other words, goinghrough the Maintenance of Certification process earlyoes not alter the 10-year validation. Diplomates certifiedrior to 1976 (the year that time-limited certificates were

nitiated) are also required to participate in MOC if theyish to maintain valid certificates.The deadline for submitting an application for Mainte-

ance of Certification is March 1, 2010. A brochure outlininghe rules and requirements for Maintenance of Certificationn thoracic surgery is available on the Board’s website atww.abts.org. For additional information, please contact

he American Board of Thoracic Surgery, 633 N St. Clair St,uite 2320, Chicago, IL 60611; telephone (312) 202-5900; fax

312) 202-5960; e-mail: info@abts.org.

Ann Thorac Surg 2010;89:1059 • 0003-4975/10/$36.00