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History of Multiple Previous Malignancies ShouldNot Be a Contraindication to the Surgical Resectionof Lung CancerPierre-Benoit Pagès, MD, Pierre Mordant, MD, Bertrand Grand, MD, Alain Badia, MD,Christophe Foucault, MD, Antoine Dujon, MD, Françoise Le Pimpec-Barthes, MD, PhD,and Marc Riquet, MD, PhD

Department of Thoracic Surgery, Georges Pompidou European Hospital, Paris Descartes University, Paris; Department of ThoracicSurgery, Cedar Surgical Centre, Bois Guillaume, France

Background. Patients with a history of previous malig-nancy are often encountered in a discussion of surgicalresection of non–small-cell lung cancer (NSCLC). Theoutcome of patients with 2 or more previous cancersremains unknown.

Methods. We performed a retrospective study includ-ing all patients undergoing resection for NSCLC fromJanuary 1980 to December 2009 at 2 French centers. Wethen compared the survival of patients without a historyof another cancer (group 1), those with a history of asingle malignancy (group 2), and those with a history of2 or more previous malignancies (group 3).

Results. There were 5,846 patients: 4,603 (78%) in group1, 1,147 (20%) in group 2, and 96 (2%) in group 3. Theproportion of patients included in group 3 increasedfrom 0.3% to 3% over 3 decades. Compared with groups

1 and 2, group 3 was associated with older age, a larger

Surgery, Georges Pompidou European Hospital, 20 rue Leblanc, 75015Paris, France; e-mail: marc.riquet@egp.aphp.fr.

© 2013 by The Society of Thoracic SurgeonsPublished by Elsevier Inc

proportion of women, earlier tumor stage, less inductiontherapy, and fewer pneumonectomies. Despite this, post-operative complications and mortality were similar ingroups 2 and 3, and higher than in group 1. Five-yearsurvival rates were 44.6%, 35.1%, and 23.6% in groups 1,2, and 3, respectively (p < 0.000001 for comparisonbetween 3 groups; p � 0.18 for comparison betweengroups 2 and 3). In multivariate analysis, male sex, higherT stage, higher N stage, incomplete resection, and studygroup were significant predictors of adverse prognosis.

Conclusions. Despite earlier diagnosis and acceptablelong-term survival, patients operated on for NSCLC after2 or 3 previous malignancies carried a worse prognosisthan did those undergoing operation after 1 malignancyor if there was no previous diagnosis of cancer.

(Ann Thorac Surg 2013;95:1000–5)

© 2013 by The Society of Thoracic Surgeons

Patients with 2 cancers occurring synchronously orsubsequently are commonly encountered today [1].

Patients with 3 or more primary cancers, 1 of which isnon–small-cell lung cancer (NSCLC), have historicallybeen described with a lower frequency [2, 3]. Howeverthese series are scarce, and the management of solidmalignancies has changed dramatically during the pastseveral decades, which raises 2 issues.

First, the age of patients with 3 or more cancers is notestablished. Older age would involve a classic time-dependent carcinogenesis, whereas younger age wouldfavor the hypothesis of a strong individual genetic sus-ceptibility leading to the development of multiple can-cers within a short period. Second, the prognostic impli-cation of lung cancer as a third cancer is open todiscussion. On 1 hand, previous cancers and treatmentsmay weaken the patient and decrease survival. On theother hand, the follow-up of previous malignancy maylead to earlier diagnosis of NSCLC and potentially tobetter survival.

Accepted for publication Nov 29, 2012.

Address correspondence to Dr Riquet, Department of General Thoracic

To address these issues, we conducted a retrospectivestudy to analyze the characteristics and prognosis ofpatients undergoing operation for NSCLC according totheir number of previous cancer diagnoses.

Patients and Methods

The clinical records of patients who underwent opera-tions for NSCLC from January 1980 to December 2009 atGeorges Pompidou European Hospital (Paris) and CedarSurgery Centre (Bois Guillaume) were retrospectivelyreviewed. The data were prospectively entered begin-ning in April 1984. The staging system was the Interna-tional Staging System for NSCLC, which was recentlymodified [4]. The preoperative workup included chestroentgenography, bronchoscopy, computed tomographyof the chest, spirometry, lung perfusion scanning, and athorough search for distant metastases (including posi-tron emission tomography in recent years). Mediastinos-copy was performed to exclude N3 disease and to con-firm N2 involvement in patients included in variousneoadjuvant treatment protocols depending on referringcenters. N3 disease and distant metastases precluded

operation.

0003-4975/$36.00http://dx.doi.org/10.1016/j.athoracsur.2012.11.072

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We analyzed the pathologic and prognostic indicatorsof survival in these patients. Patients treated for NSCLCwithout a history of another cancer were included ingroup 1 (1 cancer). Patients treated for NSCLC with ahistory of 1 other malignancy were included in group 2 (2cancers). Patients treated for NSCLC with a history of 2or more malignancies were included in group 3 (� 3cancers). A second malignancy was considered meta-chronous when it was treated before the lung cancerdiscovery and not retrospectively diagnosed on the avail-able previous imaging; it was considered synchronouswhen both malignancies were diagnosed at the sametime. The malignancies were considered to be 2 separateprimary lesions when the histologic features were differ-ent or were confirmed to be different by immunochemi-cal methods when the histologic features were similar.Questionable cases were considered to be potential me-tastases and were not included. The study was approvedby our Thoracic Surgery Society Ethic Committee, whichwaived the need for informed consent.

Follow-up information was obtained from the hospitalcase records, from a questionnaire completed by thechest physician or general practitioner, or from deathcertificates. The main outcome was the overall survival,defined as the time interval between the date of thoracicsurgical intervention and the date of death or the lastfollow-up visit for censored patients. Mean duration offollow-up was 92 � 67 months; 145 patients (2.5%) werelost to follow-up. Actuarial survival curves were esti-mated by the Kaplan-Meier method. Statistical compar-isons between survival distributions were made usingthe log-rank test. Multivariate analysis was performedusing the Cox proportional hazards model for overallsurvival analysis. Univariate analysis was performed us-ing the following outcome variables: sex, age, type ofsurgical resection, histologic features, type of N involve-ment, and type of other malignancy. All data analyseswere conducted with the 2-sided test, and a p value lessthan 0.05 was considered statistically significant. Thestatistical software used for the analysis was SEM (Anti-cancer Centre Jean Perrin, Clermont-Ferrand, France) [5].

Results

Of the 5,846 patients who met inclusion criteria, 4,603(78%) were in group 1, 1,147 (20%) were in group 2, and

96 (2%) were in group 3. In group 2, previous cancersincluded head and neck (n � 354 [6%]), lung (n � 349[6%]), hematopoetic (n � 55 [1%]), and other organs (n �389 [7%]). Group 3 patients represented 8% of the pa-tients with another malignancy (96/1,243) and 2% of theoverall study population (96/5846), but this last propor-tion increased 10-fold over 3 decades (from 0.3% to 3%).

In group 3, the total number of previous cancers was196 and included lung (n � 45 [23%]), head and neck (n �40 [20%]), urinary tract (kidney, bladder, prostate gland;n � 31 [16%]), breast (n � 21 [11%]), hematopoetic andlymphatic tissue (n � 17 [9%]), colon (n � 11 [6%]), skin(n � 6 [3%]), sarcoma (n � 2 [1%]), and miscellaneous(n � 9 [6%]). Two previous cancers were observed in 92patients and 3 previous malignancies in 4 patients. Themost common combinations seen in patients with 2previous cancers are summarized in Fig 1. In patientswith 3 previous cancers, the combination consisted oflung cancer associated with head and neck and anotherorgan in 3 patients, and urinary tract cancer, head andneck, and breast in 1 patient. The disease-free intervalbetween the previous cancer (ie, the first cancer in group2 and the second cancer in group 3) and the index lungcancer was 76 � 72 months (range, 3–468 months) ingroup 2 and 57 � 56 months (range, 3–288 months) ingroup 3.

Patient demographics and management are shown inTable 1. Briefly, compared with groups 1 and 2, patientsfrom group 3 were older, more often women, receivedless induction therapy, and underwent fewer pneumo-nectomies. Despite this, postoperative complicationswere more frequent in groups 3 (n � 28 [29.7%]) and 2(n � 264 [23%]) than in group 1 (n � 1001 [21.7%]; p �0.001). Postoperative mortality was higher in groups 3(n � 5 [5.2%]) and 2 (n � 70 [6.1%]) than in group 1 (n �165 [3.6%]; p � 0.001). However postoperative complica-tions and mortality did not differ significantly betweengroups 2 and 3 (p � 0.39).

The characteristics of the tumors are reported in Table2. Compared with groups 1 and 2, patients from group 3presented no significant difference in histologic features,but adenocarcinomas tended to be more frequent. Pa-tients from group 3 were also found to have more limitedtumor extension. The rate of tumors smaller than 3 cmwas higher in group 3 (n � 61 [63.5%]) than in group 1(n � 1930 [41.9%]; p � 0.000001) but not group 2 (n � 578

Fig 1. Most common combinations in patientswith 2 previous cancers.

(88%

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[50.4%]; p � 0.12). T1 tumors were more frequent ingroup 3 (n � 48 [50%]) than in groups 1 (n � 1179 [25.6%])and 2 (n � 315 [27.5%]; p � 0.000001). N1-2 nodalextension was less frequent in group 3 (n � 14 [14.6%])than in groups 1 (n � 2,080 [45.2%]) and 2 (n � 416[36.3%]; p � 0.000001).

Overall patient survival is reported in Table 3 and Fig2. It was lower in groups 2 and 3 than in group 1 (p �

Table 1. Patient Demographics and Management (N � 5,846

Variable Group 1

Period1980–1989 1,2011990–1999 1,8522000–2009 1,551

DemographicsFemale 841Mean age (y) 61 �

Smoker 4,140Management

Induction therapy 731Exploratory thoracotomy 209Infralobar resection 256Lobectomy 2,557Pneumonectomy (including completion) 1,581

Complete lymphadenectomy 4,067

Table 2. Patient Histologic and Pathologic Findings (N � 5,8

Variable Group 1 (n � 4,603)

Histologic typeAdenocarcinoma 1859 (40%)Squamous cell 2129 (46%)Undifferentiated large cell 373 (8%)Adenosquamous 119 (3%)Others 123 (3%)

Tumor ClassificationTx 72 (1.6%)In situ 14 (0.3%)T0 71 (1.5%)T1a 643 (14%)T1b 536 (11.6%)T2a 1,627 (35.3%)T2b 431 (9.4%)T3 919 (20%)T4 268 (5.8%)

Other noduleSame lobe 75 (1.6%)Another lobe 49 (1.1%)

NodesNx 117 (2.5%)N0 2406 (52.3%)N1 867 (18.8%)N2: 1 station 787 (17.1%)

N2: 2 stations 426 (9.3%)

0.000001), with a median survival of 47, 34, and 29 monthsfor groups 1, 2, and 3, respectively. When comparinggroups 2 and 3, there was a nonsignificant difference inoverall survival when considering the whole population(p � 0.18), but this difference became significant whenconsidering N0 patients only (p � 0.0092). In group 3,5-year survival rates were not significantly different be-tween synchronous (n � 25 [23.9%]) and metachronous

4,603) Group 2 (n � 1,147) Group 3 (n � 96) p Value

�0.01) 142 (12%) 4 (4%)) 436 (38%) 27 (29%)) 569 (50%) 65 (67%)

) 245 (17%) 29 (30%) �0.0012 63.6 � 9.3 65.9 � 8.4 �0.001

) 1,015 (88%) 81 (84%) 0.2

) 165 (14%) 4 (4%) �0.01) 22 (2%) 2 (2%) �0.000001) 177 (15%) 26 (27%) �0.000001) 688 (60%) 51 (53%) �0.000001) 260 (23%) 17 (18%) �0.000001) 753 (88%) 358 (92%) 0.089

roup 2 (n � 1,147) Group 3 (n � 96) p Value

0.23510 (40%) 46 (48%)493 (43%) 40 (42%)90 (8%) 7 (7%)22 (2%) 2 (2%)34 (3%) 1 (1%)

�0.00000111 (1%) 1 (1%)4 (0.3%) 0

14 (1.2%) 0182 (15.9%) 35 (36.5%)133 (11.6%) 13 (13.5%)394 (34.3%) 22 (22.9%)66 (5.8%) 7 (7.3%)

232 (20.2%) 14 (14.6%)114 (9.9%) 4 (4.2%)

�0.000001117 (10.2%) 4 (4.2%)103 (9%) 4 (4.2%)

�0.00000111 (1%) 1 (1%)

720 (62.8%) 78 (81.3%)194 (16.9%) 7 (7.3%)149 (13%) 6 (6.2%)

)

(n �

(26%(40%(34%

(18%10.

(90%

(16%(5%(6%(56%(34%

46)

G

73 (6.4%) 1 (1%)

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tumors (n � 71 [23.3%]; p � 0.88). In group 3, 72 patientsdied during follow-up—of lung cancer (n � 28 [38.9%]),unknown causes (n � 21 [29.2%]), nonmalignant disease(n � 19 [26.4%]), and extrapulmonary malignancy (n � 4[5.6%]).

Results of the multivariate analysis are summarized inTables 4 and 5. When considering group 1 as a referencefor the comparison between groups, male sex, pneumo-nectomy, higher T stage, higher N stage, R1 and R2resections, and groups 2 and 3 were significantly associ-ated with adverse prognoses. When considering group 2as a reference for the comparison between groups, malesex, advanced age, higher T stage, higher N stage, R1 andR2 resections, and group 3 were significantly associatedwith adverse prognoses.

Comment

In 1969, Cahan and colleagues [2] reported 113 patientsdiagnosed during a 40-year period at the MemorialSloan-Kettering Cancer Center in New York. In 1977,Sochocky and associates [3] reported 6 patients hospital-ized between 1954 and 1974 in the Veterans Administra-tion Hospital in Minneapolis. Decades later, studying the

Table 3. Survival According to the Study Group

VariableGroup 1

(n � 4,603)Group 2

(n � 1,147)Group 3(n � 96) p Value

Overallpopulation

�0.000001

5-y survivalrate

44.6% 35.1% 23.6%

10-y survivalrate

28.8% 18.2% 13.2%

N0 patients5-y survival

rate58.2% 45.3% 27%

10-y survivalrate

38.5% 22.6% 17.3%

Fig 2. Overall survival according to study group.

prognosis of patients operated on for NSCLC accordingto the number of previous malignancies they presented,we found that despite earlier diagnoses, patients with 2or 3 previous malignancies had a worse prognosis thandid those with 1 or no previous cancers.

Progressive improvements in screening, diagnosis, andmultidisciplinary management of patients with cancerhave resulted in a significant improvement in overallsurvival. In the United States, the number of cancersurvivors has tripled since 1971 and is growing by 2%each year. In 2001, there were 10 million cancer survivors,representing 3.5% of the population [1]. As a conse-quence, the number of patients presenting with multiplecancers, 1 of which is lung cancer, has increased overtime [6–8]. Second and higher order cancers now accountfor 16% of newly diagnosed malignancies reported to theUS National Cancer Institute’s Surveillance, Epidemiol-ogy, and End Results program [1]. In our surgical expe-rience, the proportion of patients with 2 or more previousmalignancies is following the same trend. This propor-tion reached 3% of surgical patients during the pastdecade and 8% of patients with previous malignancies

Table 4. Multivariate Analysis of Prognostic Factors WhenConsidering Group 1 as a Reference for the ComparisonsBetween Groups

VariablesHazardRatio

95%Confidence

Interval p Value

Male versus female 1.21 1.11–1.31 0.000007Pneumonectomy versus lesser

resection (reference)1.17 1.10–1.24 0.000001

T2 versus T1(reference) 1.29 1.23–1.34 0.000001T3 � T4 versus T1 (reference) 1.65 1.52–1.82 0.000001N1 versus N0 (reference) 1.35 1.30–1.40 0.000001N2 versus N0 (reference) 1.82 1.68–1.97 0.000001R1� R2 versus R0 (reference) 1.91 1.75–2.09 0.000001G2 versus G1 (reference) 1.40 1.31–1.50 0.000001G3 versus G1 (reference) 1.97 1.73–2.25 0.000001

Table 5. Multivariate Analysis of Prognostic Factors WhenConsidering Group 2 as a Reference for the ComparisonsBetween Groups

VariablesHazardRatio

95%Confidence

Interval p Value

Male versus female (reference) 1.42 1.20–1.68 0.00006Age � 63 y versus � 62 y

(reference)1.33 1.17–1.52 0.00002

T2 versus T1 (reference) 1.23 1.13–1.34 0.000003T3 � T4 versus T1 (reference) 1.51 1.27–1.80 0.000001N1 versus N0 (reference) 1.40 1.29–1.52 0.000001N2 versus N0 (reference) 1.96 1.67–2.31 0.000001R1� R2 versus R0 (reference) 1.77 1.44–2.17 0.000001

G3 versus G2 (reference) 1.41 1.10–1.80 0.006

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during the whole period. The same proportion has beenreported in the study by Liu and colleagues [6], includingboth surgical and nonsurgical patients, and the study ofAguiló and associates [9], including surgical patientsonly.

The physiopathologic features of multiple primarycancers remains open to discussion. On one hand, themechanism of tobacco-related carcinogenesis has beenproposed [6, 10]. The frequency of the combination ofNSCLC with head and neck [11] or urinary tract [12]malignancies supports this theory. Multiple primarylung cancers are also frequently reported, and thiscombination may even be underestimated, as samelobe or ipsilateral malignant nodules are not consid-ered multiple primary tumors in the new TNM classi-fication [4]. Furthermore, patients who smoke havebeen reported to have a significantly higher risk for thedevelopment of multiple primary malignancies involv-ing lung cancer [6].

On the other hand, there are strong clinical argumentsto minimize the role of tobacco-related carcinogenesisand to advocate the role of individual susceptibility. First,aside from NSCLC, head and neck, and bladder cancer,tobacco is involved in multiple cancers, including esoph-agus, stomach, liver, pancreas, kidney, colon-rectum, anduterine cervix, whose incidences have not been reportedto be elevated in patient with multiple primary cancersinvolving the lung [6, 10]. In our study, patients with ahistory of 2 or more previous cancers tended to beyounger than the other patients, arguing against the timedependence of tobacco-induced carcinogenesis. Lastly,this group did not have a higher proportion of activesmoking habits than did the other patients. Together,these data suggest that the carcinogenesis of multipleprimary cancers involving the lung could be induced bytobacco use, individual susceptibility, or a combination ofboth.

When considering the surgical resection of NSCLC,patients with a history of 2 or more previous cancers havea different profile than the overall population. They tendto be younger, more often women, and present morefrequently with adenocarcinomas. Nearly 3 decades ago,Watanabe and associates [7] found that squamous cellcarcinoma was the most frequent histologic type in thecase of multiple cancers. These findings have been con-firmed by more recent studies reporting adenocarcinomato be most frequent [6]. This change in cancer pathologicfindings may be linked to the modifications in cigarettemanufacturing and consumption [13–15]. Patients whohave had previous malignancies are also diagnosed ear-lier than patients who have not because of the radiologicfollow-up of their previous malignancies. Because theyare diagnosed at earlier stages, they receive less induc-tion therapy and more limited resections. This first find-ing argues for the close radiologic follow-up of patientswith solid malignancies after their treatment ends, de-spite the absence of prospective data to support thispractice [16].

Despite earlier diagnosis and less extensive resection,

patients with a history of previous cancers experienced

higher postoperative morbidity and mortality than didpatients without previous malignancies, regardless of thenumber of previous cancers. These findings reflect thepoor general status of some cancer survivors and argueagainst a potential selection bias in the study group. Afterthe initial hospitalization, the long-term prognosis ofpatients with a history of 2 or more previous malignan-cies is poor. After multivariate analysis, we confirmed aprevious history of 2 or more cancers to be an indepen-dent prognostic factor of adverse outcome after surgicalresection of NSCLC. Opposite results have been re-ported. In the studies by Aguiló and coworkers [9] in 21patients with 3 primary tumors and by Duchateau andcolleagues [12] in 34 patients with 3 primary tumors,multiple primary cancers involving the lung were actu-ally associated with a better survival than was isolatedprimary lung cancer. However both studies includedpatients with another primary tumor that occurred eitherbefore or after the lung cancer that was considered to bethe index malignancy. Therefore because patients musthave survived their lung cancer for a subsequent secondprimary tumor to develop, a strong selection bias occurs.In our experience, including only patients with a historyof previous malignancy, this fragile population is associ-ated with increased postoperative mortality and de-creased overall survival, regardless of the number ofprevious malignancies noted. However this assertion islimited by the lack of information regarding the treat-ment of previous malignancies, including previous che-motherapy and/or radiotherapy.

In conclusion, our findings suggest that despite earlierdiagnosis, patients undergoing operation for NSCLCafter 2 or 3 previous malignancies have a worse prognosisthan do those with 1 malignancy or no previously diag-nosed cancer. However surgical resection is still associ-ated with acceptable long-term survival in this patientpopulation.

We gratefully acknowledge the assistance of Dr Cara Ciprianofor her careful review and thoughtful contributions to thiswork.

References

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2. Cahan WG. Multiple primary cancers, one of which is lung.Surg Clin North Am 1969;49:323–35.

3. Sochocky S. Primary carcinoma in lung associated withprimary malignancies in other systems. Br J Clin Pract1977;31:52–6.

4. Rami-Porta R, Crowley JJ, Goldstraw P. The revised TNMstaging system for lung cancer. Ann Thorac Cardiovasc Surg2009;15:4–9.

5. Kwiatkowski F, Girard M, Hacene K, Berlie J. Sem: a suitablestatistical software adaptated for research in oncology. [Ar-ticle in French] Bull Cancer 2000;87:715–21.

6. Liu YY, Chen YM, Yen SH, Tsai CM, Perng RP. Multipleprimary malignancies involving lung cancer-clinical charac-

teristics and prognosis. Lung Cancer 2002;35:189–94.

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7. Watanabe S, Kodama T, Shimosato Y, et al. Multiple primarycancers in 5,456 autopsy cases in the National Cancer Centerof Japan. J Natl Cancer Inst 1984;72:1021–7.

8. Engeland A, Bjørge T, Haldorsen T, Tretli S. Use of multipleprimary cancers to indicate associations between smoking andcancer incidence: an analysis of 500,000 cancer cases diagnosedin Norway during 1953-93. Int J Cancer 1997;70:401–7.

9. Aguiló R, Macià F, Porta M, Casamitjana M, Minguella J,Novoa AM. Multiple independent primary cancers do notadversely affect survival of the lung cancer patient. EurJ Cardiothorac Surg 2008;34:1075–80.

10. Wynder EL, Mushinski MH, Spivak JC. Tobacco and alcoholconsumption in relation to the development of multipleprimary cancers. Cancer 1977;40:1872–8.

11. Priante AVM, Castilho EC, Kowalski LP. Second primary

Sixtieth Annual Meeting—Cal

site through the STSA website at www.stsa.org begin-

© 2013 by The Society of Thoracic SurgeonsPublished by Elsevier Inc

12. Duchateau CSJ, Stokkel MPM. Second primary tumors in-volving non-small cell lung cancer: prevalence and its influ-ence on survival. Chest 2005;127:1152–8.

13. Hoffmann D, Djordjevic MV, Hoffmann I. The changingcigarette. Prev Med 1997;26:427–34.

14. Stellman SD, Muscat JE, Thompson S, Hoffmann D, WynderEL. Risk of squamous cell carcinoma and adenocarcinoma ofthe lung in relation to lifetime filter cigarette smoking.Cancer 1997;80:382–8.

15. Wynder EL, Muscat JE. The changing epidemiology ofsmoking and lung cancer histology. Environ Health Perspect1995;103:143–8.

16. Travis LB, Rabkin CS, Brown LM, Allan JM, Alter BP,Ambrosone CB, et al. Cancer survivorship—genetic suscep-tibility and second primary cancers: research strategies and

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tumors in patients with head and neck cancer. Curr OncolRep 2011;13:132–7. recommendations. J Natl Cancer Inst 2006;98:15–25.

Southern Thoracic Surgical Association:

l for Abstracts

You are invited to submit abstracts and surgical motionpictures for the Southern Thoracic Surgical Association(STSA) Sixtieth Annual Meeting to be held October30 –November 2, 2013 at the Hyatt Regency ScottsdaleResort & Spa at Gainey Ranch in Scottsdale, Arizona.

To submit an abstract, access the online submission

ning in early February. Abstracts must be submitted byMonday, April 8, 2013 at 11:59 PM, Eastern Time.Accepted abstracts will be presented at the STSASixtieth Annual Meeting as oral presentations or sur-gical videos.

Please direct any questions regarding abstract sub-

mission to STSA at stsa@stsa.org or (800) 685-7872.

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