The Effect of Surgical Treatment on Survival from Early Lung Cancer* Implications for Screening

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1 The Effect of Surgical Treatment on Survival from Early Lung Cancer* mplications for Screening Betty J Flehinger Ph.D.; Marek Kimmel Ph.D.; and Myron R. Melamed M.D. We assessed the effect of surgery on survival from stage non-small-cell lung cancer based on data collected in these screening programs. The majority of patients diagnosed in each program were treated by surgical resection but 5 percent of the Sloan-Kettering groop 21 percent of the Hopkins groop and 11 percent of the Mayo groop failed to receive surgical treatment. Appoximately 7 percent of the stage patients in each program who were treated surgically survived more than 6ve years but there were only two 6ve-year survivors among those who did not have surgery. We conclude that patients with lung cancers detected in stage by chest x-ray ffim and treated surgically have a good chance of remaining free of disease for many years. Those stage lung cancers which are not resected progress and lead to death within 6ve years. Therefore every eftort should be made to detect and treat lung cancer early in high-risk populations. (Chellt 1992; 11:113-18) tn important and controversial question relates to 1"1 the value of periodic radiographic screening of individuals at high risk of lung cancer. There is abundant evidence that some early-stage lung cancers can be detected in the absence of symptoms by routine screening x-ray films. When cancers detected through screening are resected a large fraction of the patients remain free of disease for many years often until they die of other causes. The five-year survival of patients with stage resected lung cancer is as high as 7 percent 1 dramatically different from that observed in the general population of patients with lung cancer. This difference might be attributed to bias from two well-defined sources lead time and length-biased sampling. However if any of these effects accounted for the favorable survival one would expect that the same stage patients would have comparable survival even if they remained untreated. We demonstrate in this article that the survival is not attributable to these sources of bias. For ethical reasons no one proposes a randomized trial comparing surgery with no surgery for stage non-small-celllung cancer. However we are fortunate in having access to survival data about three groups of early lung cancer patients identified in three different institutions through similar screening procedures. The major difference among the institutions was in the fraction of detected cancers that were treated surgically. We present our analysis of comparative survival *From the Department of Mathematical Sciences BM Research Division T.J. Watson Research Center Yorktown Heights NY (Dr. Flehinger); the Department of Statistics Rice University Houston TX (Dr. Kimmel); and the Department of Pathology New York Medical College Valhalla NY (Dr. Melamed). Supported in part by American Cancer Society grant RD36. Manuscript received April 8; revision accepted July 1. &print requests: Dr. Flehinger Rm BM T. ]. Wltson &search Center Yorktown Hts New York 1598 statistics with our interpretation of the effects of surgical treatment of early lung cancer. We demonstrate that surgical treatment of stage non-small-cell lung cancer makes a large difference and that it is therefore desirable to identify early-stage disease. Previous papers have described clinical trials 1 5 investigating the early detection of lung cancer and mathematical models of the natural history of the disease.67 These trials were carried out under the auspices of the National Cancer nstitute at the Johns Hopkins Medical nstitutions the Mayo Clinic and the Memorial Sloan-Kettering Cancer Center. They were designed to investigate the efficacy of adding cytologic examination of sputum every four months to programs of periodic chest x-ray films. The Mayo Clinic study compared two groups of men all of whom were found free of lung cancer in initial screening examinations by chest radiography and sputum cytology. One group (4618 men) was offered chest x-ray films and sputum cytology every four months for six years while the other group (4593 men) received only the standard Mayo Clinic advice to be screened annually. A total of 366 lung cancers were found in these two groups in addition to 91 detected in the initial prerandomization screening. No significant difference between the two groups in lung cancer mortality was found. n a recent article 8 this result was explained with analysis that concluded "the data are consistent with the hypothesis that many of the lesions detected by screening and labeled as cancers were not clinically important in the sense that they would never have become clinically evident during the time of the clinical trial and follow-up (approximately 12 years)." The results of the present study contradict that hypothesis. n Hopkins and Sloan-Kettering where the study CHEST 11 4 APRL

2 Table 1-Number of lbtienta in Compariaon Seudg Claaljied by lrutitutiora. TNM Staging and 'lreatment Sloan-Kettering Hopkins Mayo Total Stage Surgery No Surgery Surgery Tumor Nodes Metastases TNOMO T2NOMO Total stage TMO+T2MO TN1MO T2NMO TN2MO T2N2MO Total TMO+T2MO 152 S 159 No Surgery Surgery No Surgery Surgery No Surgery designs were almost identical approximately 1 volunteers male smokers aged 45 and older with no history of lung cancer were enrolled by each instutition. All were offered annual radiographic examinations and half were asked to submit sputum specimens for cytologic examination every four months starting at enrollment. All patients with lung cancer detected through screening or outside the screening program were given the recommendation of surgical resection whenever that treatment was considered feasible. All participants were offered screening examinations for at least five years plus at least two years of follow-up examinations. The total numbers of cancers documented in all groups were 484 in the Hopkins study and 354 in the Sloan-Kettering study. t has been reported that although sputum cytology detects some early cases of epidermoid carcinoma of the lung it does not induce a significant improvement in lung cancer mortality when added to annual chest x-ray film examinations. (See reference 1 for discussion.) Since all participants at Hopkins and Sloan-Kettering received annual chest x-ray films there was no direct evidence from these institutions about the effect of radiographic screening on lung cancer mortality. A careful review of data gathered by all three institutions has revealed that a sizeable number of stage cancers failed to be resected either because patients refused surgery or because the surgeons believed that there were medical contraindications to surgery. The proportions of patients who failed to be treated surgically varied from 5 to 21 percent. Since these were all stage cancers the decisions not to operate were in no case related to the resectability of the tumor. Therefore a comparison of times to lung cancer death in surgical vs nonsurgical cases sheds light on the efficacy of surgical treatment of early lung cancer. We present the results of these comparisons and discuss the implications of these results with respect to lung cancer screening and treatment decisions. BACKGROUND AND METHODS By direct access to the computer-based files of the Mayo Hopkins Table!-Number of lbtienta in Compariaon Seudg Claaljied by lrutitutiora. Cell]}lpe and 'lreatment Sloan-Kettering Hopkins Mayo Total Stage Surgery No Surgery Surgery No Surgery Surgery No Surgery Surgery No Surgery Cell type Adenocarcinoma SS 11 Epidermoid Large cell Other non-small cell lung cancer Total stage All TMO+T2MO Cell Type Adenocarcinoma Epidermoid Large cell Other non-smallcell lung cancer Total 152 S SUigary Elfacta on SUrvival from Early Lung Cancer (Fielllngec Kimmel Me/emed}

3 and Sloan-Kettering early lung cancer detection studies we identified all cases of stage (TNOMO T2NOMO)" non-small-ceo lung cancer diagnosed in the years 1974 to 1984 in the populations enrolled in the studies. Because they were not detectable by chest x-ray films we did not include any tumors found solely by sputum cytology. For each identified case we determined whether the patient was surgically explored and the tumor resected. The staging (tumor nodes and metastases) cell types and treatments of the populations are tabulated in 'llbles 1 and 2. The Sloan-Kettering group of stage patients consisted of 98 men of whom 95 percent had their tumors resected. This surgical group ranged in age from 45 to 77 years old with the median age being 59 years old while the five nonsurgically treated patients ranged in age from 56 to 73 years old with the median age being 72 years. Three of them considered inoperable for medical reasons were treated with radiotherapy and two refused surgery. The Hopkins stage group had 137 members 79 percent of whom had operations. These 18 surgically treated men were 46 to 76 years old with the median age 6; the 29 nonsurgically treated patients were 51 to 77 years with the median age 66 years. Fifteen of them were considered inoperable fur medical reasons; seven of these received radiotherapy and 14 refused surgery. The Mayo group of stage patients had 96 members of whom 85 or 89 percent were treated surgically. They ranged in age from 5 to 76 years old with the median age being 66 years while the 11 men who did not undergo surgery were 47 to 75 years old with the median age being 66 years. Ten of them considered inoperable for medical reasons received radiotherapy while one refused surgery. n all three centers patients whose cancers were completely resected received no additional treatment. We estimated the survival probability after detection (Kaplan- Meier product-limit estimates) fur the Sloan-Kettering Hopkins and Mayo stage populations segregated according to whether or not they were treated surgically. As endpoints for this analysis we used death due to lung cancer including postoperative deaths. Every death of a man enrolled in this program had been reviewed by a committee of chest physicians and pathologists from all three institutions who met every four months to examine all records and to determine whether death was due to lung cancer. The statistical significance of all survival comparisons was computed by both the log-rank test and the modified Wilcoxon test. We were concerned that bias might be introduced into this analysis by the fact that some cases clinically classified as stage might have had unrecognized nodal involvement. f operations had not been done they would have been understaged. Therefore we repeated the analysis described previously fur all patients with tumor stage T1 or T2 with no distant metastases regardless of nodal status. The characteristics of these enriched comparison groups are tabulated in the lower halves of'llbles 1 and 2. The enriched group SLOAN-KETERNG q - HOPKNS PLR =.45 Pw=.2 1 _ SURGERY(98) NO SURGERY(5) _ YEARS FROM DETEC11N -1 - PLR =.2 Pw<.1 1_ 1.. SURGERY(1 8) NO SURGERY(29) _ YEARS FROM DETEC11N MAYO PLR =.2 Pw=.1 SURGERY(85) NO SURGERY( 11) _ _ YEARS FROM DETEC11N FtcuRE 1. Kaplan-Meier estimates of survival from stage (T1NOMO and T2NOMO) lung cancer. Deaths are due to lung cancer. Deaths from other causes are treated as withdrawal. Puc= significance for the logrank test; P ww =significance fur the modified Wilcoxon test. CHEST 11 4 APRL

4 1:; ;; a - - T1NOMO T2NOMO T1 N ANYMO T2NANYM SURGERY(291) SURGERY( 434).. '.. '' L - 1:; NO SURGERY( 45) -. 1 '.. L ;; ' -.NO SURGERY(92) ---_ -- a '-- PLR =.2 ' PLR < FW <.1 FW < Ll YE'ARS FROM DET CT1N YE'ARS FROM DET CT1N FGURE 2. Kaplan-Meier estimates of survival from Tl Nany MO and T2 Nany MO lung cancer. Deaths are due to lung cancer. Deaths from other causes are treated as withdrawal. Puc== significance for the log-rank test; P... ==significance for the modified Wilcoxon test. "---.. SLOAN-KETTERNG HOPKNS 5 1:; ;; a ' SURGERY (152) SURGERY (159) --1 NO SURGERY (15) NO SURGERY (55) PLR =.7 PLR=.5 A.tw<.1 1 Pww<.1 '--. a ' YE'ARS FROM DET CT1N YE'ARS FROM OETECfiON MAYO SURGERY ( 123) _ 1 NO SURGERY (22) PLR =.4 Pww<.1 _ _ YE'ARS FROM DET CT1N FGURE 3. Kaplan-Meier estimates of survival from lung cancer in total surgical and non-surgical samples. Deaths are due to lung cancer. Deaths from other causes are treated as withdrawal. Puc==significance for the log-rank test; P... ==significance for the modified Walcoxon test. 116

5 contains those stage and patients who would be considered stage if it were not for nodal involvement. The Sloan-Kettering population was increased by 64 cases 54 of which were explored surgically; the Hopkins group was increased by 77 cases 51 of which were explored; the Mayo group was increased by 49 cases 38 of which were explored surgically. RESULTS The estimated survival distributions are plotted in Figures 1 to 3 and the five-year survivals are summarized in Table 3. First for the stage patients we compared survival after surgery with survival of those who were not treated surgically in Sloan-Kettering Hopkins and Mayo (Fig 1). We considered only lung cancer deaths including three postoperative deaths in Sloan-Kettering two in Hopkins and two in Mayo as endpoints. Deaths from other causes were treated as withdrawals. The five-year survival probabilities after surgery ranged from 63 to 76 percent the curves exhibiting no statistically significant differences among institutions. The five-year survival probabilities of the nonsurgical patients ranged from to 19 percent again with no statistically significant differences among the institutions. The significance values associated with the contrasts between surgical and nonsurgical groups are indicated in Figure 1. The modified Wilcoxon test indicated significant differences in all three institutions but the numbers of patients who failed to be explored surgically at Memorial and Mayo were too small to provide significance in the log-rank test. We note that there were no five-year survivors in the nonsurgical group at Sloan-Kettering one at Hopkins and one at Mayo. Figure 3 exhibits the contrast between survival estimates based on the total samples from the three institutions surgical and nonsurgical. Here both significance tests indicate significant differences. Comparisons based on deaths from all causes sharpen the contrasts between surgical and nonsurgical groups. These results are not reported here because of the obvious bias introduced by the fact that those patients considered inoperable were likely to Kettering population there were 7 cases detected by routine screening x-ray films and 28 interval and postscreening cases; in Hopkins the corresponding numbers were 91 and 17; in Mayo they were 29 and 56. The excess number of interval cases at Mayo may be explained by the fact that the Mayo control group received no routine screening x-ray films. Only the Mayo patients exhibited a significant difference based on the mode of detection and further analysis demonstrated that of the 56 interval cases 26 were treated at a variety of hospitals outside the Mayo Clinic. The 3 interval cases treated at Mayo had a survival curve almost identical to the screening-detected cases while the 26 treated outside had markedly poorer survival. We concluded that the survival of true stage patients (T1NOMO and T2NOMO) surgically resected in teaching hospitals has little dependence on mode of detection. Staging was necessarily clinical for patients who did not have operations whereas it was pathologic staging for those who did have operations. To assure that the difference in staging did not induce bias by understaging (clinical) of patients who were not treated surgically we repeated all the analyses for the enriched groups consisting of all T1MO and T2MO cancers regardless of nodal status. The results are qualitatively identical with those for stage patients (Fig 2 and 3). Five-year survivals (with lung cancer death as an endpoint) for those who were operated on ranged from 52 to 62 percent while for those who did not undergo surgery survival ranged from to 8 percent. Once again there was no statistically significant difference in the treatment-specific survival curves among institutions; the paired comparisons by treatment are indicated on the graphs and because of larger sample sizes exhibit more significance than do the stage comparisons. DiscussiON die of causes other th lung cancr. Patients in this study with lung cancer detected. We_ compared uj"vvals of surgtcal stage patients early who were untreated died oflung cancer; patients dentified by rotine scening x-ray films with interval with lung cancer detected early who were treated by and post-screemng surcal stage cases. n the Sloan- resection of their tumor had a high probability of Table 3-Numbera oflbtienta and Five-Year Survioal ProbtJbiUtia (Kaplan-Meier &timotea) Clauijied by lrutitution Stage and Sloan-Kettering Hopkins Mayo Total Stage (flnomo and T2NOMO) Surgical population Survival probability 76% 69% 63% 7% Non-surgical population Survival probability % 9% 19% 1% All T1MO and T2MO Surgical population Survival probability 62% 53% 52% 57% Non-surgical population Survival probability % 8% 8% 7% CHEST 11 4 APRL

6 survival. Survival from stage lung cancer for surgically treated patients ranged from 63 to 76 percent at five years; for the cases not treated surgically the range was to 19 percent with only two survivors among the 45 cases not treated surgically at the three institutions. By definition stage lung cancer is resectable. However not all patients with stage 1 cancer were operated on. The decision not to operate on stage 1 lung cancers was based on the patients refusal or the surgeons evaluation of the patient's ability to survive surgery. The extent of the cancer played no role in the decision. f it were true that a substantial number of x-ray film-detectable lung cancers would remain dormant for many years untreated then a substantial proportion of the 45 untreated stage 1 patients would have survived from lung cancer for more than five years. Unfortunately the methods available for detection of early lung cancer at this time are not highly sensitive. n a mathematical modeling study 7 we estimated that sensitivity of x-ray film detection of stage tumors is at most 16 percent. However it is clear from the results of this study that the treatment of lung cancer detected early is effective. Survival following surgical resection of stage lung cancer is approximately 7 percent at five years; whereas only two patients out of 45 with unresected stage lung cancer survived for five years. This provides strong evidence for the concept that early lung cancers detected by x-ray film will progress and cause death if untreated. Nearly identical survival curves were obtained from three institutions with striking differences between groups of patients who were and were not treated surgically. We have previously urged that annual chest x-ray films be used to detect early lung cancer in subjects at high risk of the disease. 1 Admittedly the chest x-ray film is not an efficient detection technique 1114 yet it is the best inexpensive and harmless technique presently available. This study provides strong support for the principle of early detection and early treatment of lung cancer. t also emphasizes the need for a concerted effort to improve the present detection techniques. ACKNOWLEDGMENTS: We thank Dr. Philip Prorok of the National Cancer nstitute for supplying us with data about the surgical treatment of Johns Hopkins patients. We also acknowledge extensive data analysis carried out by 'lltyana Polyak and manuscript preparation by Margaret Cargiulo. REFERENCES 1 Melamed MR Flehinger BJ Zaman MB Heelan RT Perchiclt WA Martini N. Screening for early lung cancer: results of the Memorial Sloan-Kettering study in New York. Chest 1984; 86: Berlin N Buncher CR Fontana RS Frost JK Melamed MR. The National Cancer nstitute Cooperative Early Lung Cancer Detection Program: results of the initial screen (prevalence): early lung cancer detection: introduction. Am Rev Respir Dis 1984; 13: Flehinger BJ MelamedMR Zaman MB Heelan RT Perchick WB Martini N. Early lung cancer detection: results of the initial (prevalence) radiologic and cytologic screening in the Memorial Sloan-Kettering study. Am Rev Respir Dis 1984; 13: Fontana RS Sanderson DR Taylor WF Woolner LB Miller WE Muhm JR et al. Early lung cancer detection: results of the initial (prevalence) radiologic and cytologic screening in the Mayo Clinic study. Am Rev Respir Dis 1984; 13: Frost JK Ball WC Levin ML Tockman MS Baker RR Carter D et al. Early lung cancer detection: results of the initial (prevalence) radiologic and cytologic screening in the Johns Hopkins study. Am Rev Respir Dis 1984; 13: Flehinger BJ Kimmel M. The natural history oflung cancer in a periodically screened population. Biometrics 1987; 43: Flehinger BJ Kimmel M Melamed MR. Natural history of adenocarcinoma-large cell carcinoma of lung: conclusions from screening programs in New York and Baltimore. J Natl Cancer nst 1988; 8: Eddy DM. Screening for lung cancer. Ann ntern Med 1989; 111: Mountain CF. A new international staging system for lung cancer. Chest 1986; 89:225S-33S 1 Melamed MR Flehinger BJ FOntana RS. Should asymptomatic cigarette smokers have annual chest x-rays after age 55 years? n: Gitnick G Barnes Hv Duffy TP Lewis RP Winterbauer RH eds. Debates in medicine volume 3. Chicago: Year Book Medical Publishers 199:12(H;O 11 Brett GZ. Earlier diagnosis and survival in lung cancer study. Br Med J 1969; 4:2 12 Nash FA Morgan JM Tomkins JG. South London lung cancer study. Br Med J 1986; 2: Weiss W. Boucot KR Seidman H. The Philadelphia pulmonary. research project. Clin Chest Med 1982; 3: Fontana RS Sanderson DR Woolner LB 'llylor WF Miller WE Muhm JR. Lung cancer screening: the Mayo program. J Occup Med 1986; 28: Surgery Ellec:B on SUrvival from Early Lll"lg cancer (Fie/rlnge( Kimmel Melamed)

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