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Ann Thorac Surg 1995;59:863-867
© 1995 The Society of Thoracic Surgeons

Second Primary Lung Cancer

Tamim Antakli, MD, Robert F. Schaefer, MD, Jerry E. Rutherford, BS, Raymond C. Read, MD

Surgical Service and Pathology and Laboratory Medicine Service, John L. McClellan Memorial Veterans Hospital and the University of Arkansas for Medical Sciences, Little Rock, Arkansas


   Abstract
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 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
We reviewed our experience with second primary lung cancer (SPLC) at the Little Rock Veterans Affairs Medical Center from 1966 to 1993. Fifty-four patients were found to have 65 such lesions after 1,572 ``curative'' resections for lung cancer (4.1%). Eleven patients had at least a third primary tumor (3 having more). Metachronous SPLCs comprised 60% (39/65) and synchronous 40% (26/65). The mean interval between first and second tumors was 54.63 +/- 8 (standard error) months (range, 5 to 218 months), and that between second and third was 26.1 +/- 7.4 (standard error) (range, 5.5 to 51 months). Squamous cell carcinoma comprised 58.4% (38/65), adenocarcinoma 30.8% (20/65), and small cell carcinoma 10.8% (7/65). Histology of the SPLC was the same as that of the first tumor in 50.7% (33/65). Stage I primary tumors comprised 76% (41/54) of index tumors, 61.1% (33/54) of SPLCs, and 72.2% (8/11) of third primary tumors. Second primary lung cancer followed minimal resection in 44% (24/54), lobectomy in 37% (20/54), and pneumonectomy in 13% (7/54) of cases. There was no evidence that minimal resection for the first primary tumor predisposed to SPLC. After 1983 the majority of SPLCs were diagnosed with computed tomographic scanning. After resection of SPLCs, survival rates at 3 and 5 years were 26% and 18%, metachronous 39% and 23.4%, and synchronous 12.25% and 12.25%.


   Introduction
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 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
See also page 867.

The incidence of second primary lung cancer (SPLC) ranges from 0.5% to 10% [1–9]. Despite a recently reported increase, this entity is still relatively rare compared with second primary tumors in other paired organs such as the breast and ovary [1, 10]. The purpose of this report is to detail our experience with SPLC at the Little Rock Veterans Affairs Medical Center over the last 28 years.


   Material and Methods
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 Abstract
 Introduction
 Material and Methods
Results
 Comment
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Patients who underwent potentially curative lung resections for bronchogenic lung cancer in our institute between the years 1966 and 1994 were reviewed. Those with multiple pathologic specimens or one with two or more distinct lesions were selected out. Histopathology and cytology slides were studied without knowledge of the previous reports. Operative reports and tumor registry data were examined. A set of criteria modified from Martini and Melamed [3] then were applied to differentiate between second or multiple primary lung cancers and recurrence or satellite nodules:

  1. Different histology
  2. Same histology with two or more of the following:
    1. Anatomically distinct
    2. Associated premalignant lesion
    3. No systemic metastases
    4. No mediastinal spread
    5. Different DNA ploidy

In the case of identical histology at least two of these criteria had to be met. In cases of mixed histology the tumor was classified according to the predominant type. Large cell carcinoma (1 case) was counted under adenocarcinoma. One specimen had to be derived from a potentially curative resection with the exception of 2 patients who had prolonged survival after biopsy and laser treatment in 1 and chemotherapy in the other. Synchronous SPLC was identified if there was radiographic evidence of the second primary tumor at the time of first resection, or if the second primary tumor was discovered incidentally during operation or in the resected specimen. An SPLC discovered later was labeled metachronous. All data were expressed as mean +/- standard error when appropriate. Incidences of events in different groups were compared using the {chi}2 test. Survival data were analyzed using actuarial life-table analysis.


   Results
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 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Between 1966 and 1994, 1572 ``curative'' lung resections were undertaken at the Little Rock Veterans Affairs Medical Center. Fifty-four patients were found to have 65 second or up to five primary lung neoplasms. Hence, the incidence of multiple primary lung cancer was 4.1% (65/1572). Eleven patients had third primary tumors (11/65, 16.9%); 3 had more than three primary tumors (3/65, 4.6%), and 1 patient harbored four synchronous SPLCs, metachronous to a histologically different first primary cancer. The interval between the first primary tumor (also called index tumor) and the SPLC was 54.63 +/- 8 months (mean +/- standard error) (range, 5 to 218 months); that between a SPLC and a third primary cancer was 26.1 +/- 7.4 months (mean +/- standard error) (range, 5.5 to 51 months). There was a biphasic peak incidence of SPLC at 3 and 5 years after resection of the index tumor. More than 90% of SPLCs in our institution were reported after 1985 with obvious preponderance after 1989. Overall, the calculated incidence of SPLC per patient-year was 0.99%; however, data after computed tomographic scanning (1985) raise this to 6.8% (59/869). All patients except 1 were men. Average age at presentation of the first primary cancer was 64.2 +/- 1.1 years (mean +/- standard error). A smoking index (cigarettes/day x years) of more than 500 at the time of presentation with the second primary cancer was documented in 42 patients (78%); it was unknown in 6.

Metachronous SPLCs comprised 39/65 (60%) and synchronous SPLCs 26/65 (40%). A third metachronous tumor was seen in 5 and a third synchronous lesion in 6 patients. Squamous cell carcinoma made up 30/54 (55.7%) of index tumors and 38/65 (58.4%) of SPLCs. Adenocarcinoma was seen in 42.5% of index tumors (23/54) and 20 SPLCs (30.8%); small cell carcinoma arose in 1 index tumor and 7 SPLCs (10.83%). In 1 patient an adenocarcinoma developed 8 years after a peripheral small cell cancer had been resected. The histology of SPLC was the same as that of the index tumor in almost half (33/65). Stage I in the index tumors made up 76%. It comprised 61.1% (33/54) of SPLCs and 72.7% (8/11) of third primaries (Table 1Go). By far the most common location of a first and second primary tumor was the left upper lobe, 40.7% and 26%, respectively. The second most common location of SPLC was the left lower lobe. The right upper lobe was the most frequent site of a third primary cancer (Table 2Go). The SPLC was on the same side as the index tumor in 53.7% (29/54) and in the same lobe in 13% (7/54). Metachronous lesions were less likely than synchronous lesions to be in the same lung, 13/39 (33.4%) versus 12/26 (46.2%), or in the same lobe, 4/39 (10.2%) versus 4/26 (15.4%).


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  		Table 1. . Stage of Second Primary Lung Cancer in 54 Patients
 

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  		Table 2. . Loci of Second Primary Lung Cancers (n = 54)
 
In metachronous tumors all patients with the exception of two (37/39, 94.8%) had their SPLCs discovered by chest roentgenography and computerized tomography. Sputum cytology and autopsy were helpful in 1 patient (1/39, 2.6%). Twenty-one of the synchronous SPLCs (80.77%) were detected preoperatively by chest roentgenography and chest computed tomography, the rest being discovered incidentally in the resected specimen. Staged resection was performed on 53.8% of synchronous lesions (14/26) because they were contralateral to the index tumor. The most common resection of index tumors was mini-resection (wedge resection and segmentectomy), being performed in 48.7% of metachronous index tumors (19/39) and 38.4% of synchronous index tumors (10/26). Next in frequency in metachronous index tumors was lobectomy (41.4%). Lobectomy and pneumonectomy shared a rate of 27% (7/26) for synchronous index tumors (Tables 3, 4GoGo). Overall, during the study period lobectomies were carried out in 655/1572 (41.6%), mini-resections in 555/1572 (35.3%), and pneumonectomies in 262/1572 (23.1%) patients. A {chi}2 analysis was used to compare risk of SPLC with type of lung resection conducted for index tumors. There was no significant difference in risk of SPLC between mini-resections and lobectomies. ({chi}2 = 1.035; p = 0.3). The risk after pneumonectomy was, however, significantly lower than after lobectomies or mini-resections ({chi}2 = 5.027; p = 0.025). More than half the resections for SPLCs, metachronous and synchronous, were mini-resections; biopsy only could be accomplished in 30.7% of metachronous lesions and pneumonectomy in 23% of synchronous SPLCs (6/26).


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  		Table 3. . Lung Resections for Metachronous Second Primary Lung Cancers (n = 39)
 

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  		Table 4. . Lung Resections for Synchronous Second Primary Lung Cancer (n = 26)
 
Actuarial life-table analysis was used to calculate the probability of survival. The rate for all stages of SPLC was 24% at 3 years and 14.4% after 5 years. Patients with resected SPLCs had 25.7% and 18% survival rates for 3 and 5 years, respectively. Patients with stage I SPLC had survival rates of 28.3% for 3 years and 19% for 5 years. In comparison, the corresponding rates in all stage I primary lung cancers were 37% and 26% in our institution. Resected metachronous tumors had better prognoses than synchronous, 39% versus 12.25% at 3 years and 23.4% versus 12.25% after 5 years. There was no significant difference in survival probability between small cell carcinoma and adenocarcinoma (Table 5Go; Figs 1, 2GoGo).


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  		Table 5. . Survival After Second Primary Lung Cancer
 


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  		Fig 1. . Survival with all stages of second primary lung cancer.

 


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  		Fig 2. . Survival after metachronous ({blacktriangleup}, n = 39) versus synchronous (•, n = 26) second primary lung cancer.

 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Second primary lung cancer is an uncommon entity compared with multiple primary cancers from other paired organs such as the ovary and breast [1, 10]. This is interesting because all the lung tissue is exposed to carcinogenic factors. Obviously, the patient has to survive long enough after the first primary tumor in order for the second to develop [6]. Our work and that of other authors show that the peak incidence of SPLC is somewhere between the third and eighth postoperative year [4, 5, 11]. Because most lung cancer deaths occur within 2 or 3 years, a large number of patients who harbor a subclinical SPLC would be eliminated [6]. The obvious preponderance of early disease in the index tumor in our series and those of others [12, 13] attests to these assumptions. Second primary lung cancer first was reported by Beyreuther in 1928 [2]. A few other cases appeared later in the extensive review in 1932 by Warren and Gates [14] of multiple primary tumors. Martini and Melamed [3] in 1975 outlined the criteria for differentiation between SPLC and recurrence, which have been used by most subsequent authors, including ourselves.

The reported incidence has increased steadily, presumably because SPLC has been separated out from recurrence and satellite disease [1–9]. The striking prevalence of smoking among the patients in our series also has been reported by others [5, 7, 15]. This probably accounts for a continuing high proportion of squamous cell cancers (index and SPLC) in our series. Abbey-Smith and associates [5] and Richardson and colleagues [15] demonstrated the preventive effect of cessation for SPLC. It seems logical that cancerous changes of respiratory epithelium would be multicentric in response to a field effect of carcinogens. Pathologic observations in resected specimens have demonstrated this clearly, and have proved that the incidence of occult SPLC in resected specimens is considerable [16–18].

The incidence of SPLC in our series is similar to that in the literature, as are the distribution of metachronous versus synchronous lesions, histologic patterns, stages, and survival figures [3, 4, 7, 12, 19–21]. Mini-resections have been used frequently in this institution because elderly veterans have limited pulmonary reserve. However, mini-resection did not predispose our patients to higher rates of SPLC compared with lobectomies. A lesser resection on the first occasion would leave the patient with more lung tissue to resect should a second primary develop later. Pneumonectomy was found to decrease the chance of an SPLC significantly; presumably by eliminating ipsilateral metachronous lesions, which otherwise account for about half the incidence. Pneumonectomy was more common among patients with synchronous lesions because it was preferred when two separate cancers arose in the same lung. Biopsy only was used in advanced stages.

The survival advantage of metachronous compared with synchronous lesions also has been reported by others [12, 22, 23]. This difference persists even when resected lesions are considered separately. Others also have shown that survival improves as the interval between index and metachronous tumors increases [19]. The inferior survival rate of SPLC compared with first primary cancers might be related to understaging because of technical difficulties during the second or third procedure and to resorting to lesser resections because of limited pulmonary reserve. Further, a third of these SPLCs overall were unfit for anything more than biopsy. Survival rates, however, after SPLC still remain higher than those reported after recurrence [13].

More than 90% of the cases in our institution were detected within the last 8 years. The introduction of chest computed tomography in 1983 increased awareness of this entity; a more aggressive attitude toward any change in symptomatology, radiology, or cytology also is responsible. Our use of ultrastructural, histochemical, and DNA flow cytometry techniques helped to differentiate SPLCs from recurrences when Martini and Melamed's criteria were inconclusive. Others also have used these modalities [9, 24, 25]. The question of whether a newly discovered lung lesion after curative resection is actually an SPLC or a recurrence remains a theoretical one. We follow the policy of thoroughly restaging all such lesions and operating with the intention to cure whenever possible.

We conclude that SPLC is frequent in long-term survivors after curative resections. A high level of awareness and the use of computed tomography scan allow their early detection. Mini-resections have not been found to increase the risk of SPLC, and they may be preferred in patients with limited lung tissue reserve. Follow-up after lung resection should be for life because SPLC incidence increases in long-term survivors after curative resection of index or second primary lung cancer. We perform chest roentgenography and thorough clinical evaluation on each visit, and in the presence of any abnormality follow with computed tomographic scan and sputum cytology, bronchoscopy, or both. Smoking cessation should be stressed. Second primary lung cancers should be treated aggressively as the survival rate after resection of metachronous lesions is better than that after recurrence.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Presented at the Forty-first Annual Meeting of the Southern Thoracic Surgical Association, Marco Island, FL, Nov 10--12, 1994.

Address reprint requests to Dr Read, Surgical Service (112 LR), John L. McClellan Memorial Veterans Hospital, University of Arkansas for Medical Sciences, 4300 W 7th St, Little Rock, AR 72205.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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