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Eur J Cardiothorac Surg 2002;21:527-533
© 2002 Elsevier Science NL

The management of second primary lung cancers. A single centre experience in 15 years

Division of Thoracic Surgery, Hairmyres Hospital, East Kilbride, Scotland G75 8RJ, UK

Received 14 November 2001; received in revised form 28 December 2001; accepted 3 January 2002.

* Corresponding author. Tel.: +44-1355-584-661; fax: +44-1355-584-473
e-mail: letitia.evans{at}laht.scot.nhs.uk

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusions References

 
Objective: In patients treated for an initial lung cancer, the cumulative risk of developing a second primary lung cancer is a recognised occurrence. This study reviews our experience in the clinical assessment and surgical management of second primary lung cancer (SPLC). Methods: Between 1985–1999 a series of 892 patients with primary carcinoma of lung underwent surgical resection with curative intent in our institution. Using criteria set out by Martini and Melamed (J Thorac Cardiovasc Surg 70 (1975) 606) we were able to identify 51 patients who had developed a SPLC identified as the first site of re-occurrence. Results: Forty-one patients developed a metachronous SPLC within a mean of 46±14 months of the first operation while ten patients had synchronous double lung cancer (six unilateral, four bilateral). The cumulative probability of cancer free interval for metachronous cancers was 39% at 3 years, 15% at 5 years and 2% at 10 years. There were three postoperative deaths among the metachronous cancers (7.5%) and there were no operative deaths among patients with synchronous cancers. The overall actuarial 5-year survival for all patients with SPLC was 38% with a median survival of 40 months (range 1–142 months). The actuarial 5-year survival for metachronous SPLC was 44%, median survival of 49 months (range 1–142 months), while the actuarial 5-years survival for synchronous SLPC was 10% with a median survival of 31 months (range 4–78 months). Conclusion: Aggressive assessment and surgical intervention is safe, effective and warranted in patients with a second lung primary cancer if they satisfy the usual criteria of operability after full assessment. This is true for patients with metachronous cancers, while patients with synchronous cancers tend to have worse prognosis. A long term follow-up policy after the initial resection of the primary lung cancer is recommended at intervals of 6 months for at least 3–5 years and then annually to enable the early detection of the second cancer.

Key Words: Lung cancer • Second lung primary cancer

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusions References

 
The idea of multiple lung cancer was first described by Beyreuther [1] in 1924 and has been generally accepted, but the prevalence remains largely unknown. It is generally thought to vary from 1 to 10% for synchronous and metachronous cancers together. Recently reported increase in incidence probably is a result of longer survival after resection of the primary and improvements in early detection methods. Nevertheless this entity is still relatively uncommon compared with second primary tumours in other paired organs such as the breast and ovary [2,3]. Establishing appropriate criteria for assessment and management of second primary lung cancer (SPLC) is critical in distinguishing between synchronous or metachronous SPLC on the one hand and metastatic or locally recurrent primary disease on the other. This distinction can have important clinical and therapeutic implications. Pulmonary resection remains the most effective treatment modality for patients with initial or second primary lung cancer with satisfactory survival outcome. The purpose of this study is to detail our experience of clinical assessment and operative management of second primary lung cancer (SPLC) at the Hairmyres hospital over the last 15 years.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusions References

 
2.1. Patients
Patients who underwent potentially curative lung resection for non-small cell lung cancer in our institute between December 1985 and November1999 were reviewed and charts of patients with a probable diagnosis of multiple primary lung cancer analysed. The criteria based on and modified from those of Martini and Melamed [4], have been used for designation of multiple primary lung cancer (Table 1). Patients who did not meet these criteria were excluded.

All patients who underwent resection for a primary lung cancer were followed up after 6 weeks, 3 months, and then 6 monthly for 3 years and then annually till the patient's death. They get a chest roentgenogram in addition to a history and physical examination at each follow up visit. Patient with abnormal chest radiographs, symptoms or positive physical findings were further investigated by CT of the chest and upper abdomen and other investigations as appropriate.

2.2. Methods of diagnosis
Synchronous SPLC was considered if there was a radiographic evidence of the second lung primary tumour at the time of first resection, or if the second tumour was discovered incidentally during surgery or by the Pathologist in the resected specimen. The larger of two synchronous tumours was considered the first primary cancer for the purpose of this analysis. Seven of the synchronous tumours (70%) were detected on preoperative radiography or bronchoscopy and three (30%) were discovered during operation. All the metachronous SPLC lesions were discovered by chest radiographs during routine follow up and confirmed by CT. The diagnosis was established in SPLC patients who were unfit for curative surgical resection by bronchoscopic biopsy or CT guided lung biopsy. Full assessment of operable patients included bronchoscopy, mediastinoscopy, full lung function tests and brain and bone scans to rule out metastases

2.3. Follow up and data analysis
Follow up was complete up to December 1999. Operative mortality included deaths from all causes occurring within 30 days of surgery or beyond 30 days during the same hospitalisation. The interval between metachronous cancers was calculated from the date of resection of the primary tumour to the date of pathologic diagnosis of SPLC. Survival interval was calculated from the date of the second operation to the date of the last follow up or death. All data were expressed as mean±standard deviation where appropriate. Incidence of events in each group was compared by ² test. Survival incidence was calculated from the date of the second operation to the date of the last follow up or death. Cumulative survivals were calculated by the Kaplan–Meier actuarial method with the date of second operation as the starting point, and included death from all cancers. The differences in survival were determined by log-rank analysis and Wilcoxon rank test was used to compare the intervals between the first and second metachronous cancer. A P value of <0.05 was considered statistically significant.

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusions References

 
From January 1986 to June 1999, 892 patients underwent resection with curative intent for a primary lung cancer at our centre. Fifty-one (5.7%) were picked up to have a second primary lung cancer; and one of these later had a third tumour (Carcinoid) (Fig. 1) . All patients were smoking at the time of diagnosis of the synchronous cancers, and despite a strong anti smoking policy after the first operation all those who developed a metachronous SPLC had gone back to the smoking habit. Forty-one patients developed a second cancer within 20–110 months of the first operation (mean 46±14 months). The cumulative probability of cancer free interval for metachronous cancers was 39% at 3 years, 15% at 5 years and 2% at 10 years. Overall follow up ranged from 6 to 156 months with a mean of 67±22 months.

View larger version (9K): [in this window] [in a new window]   Fig. 1. The overall actuarial survival of 51 patients with synchronous and metachronous second primary lung cancer.

3.1. Location of cancers
Metachronous lesions presented in the contralateral lung in 28 of the 41 patients (68%) with a higher prevalence in the upper lobes, while six of the ten (60%) synchronous lesions were unilateral with a higher prevalence for the upper lobes. The most common location of a primary and second lung cancer was left upper lobe in 39 and 30%, respectively. The second most common location was right upper lobe.

3.2. Metachronous carcinomas
Metachronous tumours developed in 41 of 892 (4.5%). The average age at time of treatment for the first tumour was 58±6.7 years with an age range of 36–70 years, and for the second tumour was 64±6.9 years with an age range of 39±75 years, respectively. Thirty-seven patients were male. The mean interval between the initial treatment and SPLC was 46±14 months ranging from 20 months to 6.5 years. One patient developed a third lung tumour (carcinoid) 15 months after a metachronous SPLC.

3.3. Synchronous carcinomas
Synchronous tumours comprised ten of 892 (1.2%). The average age at the initial treatment was 54±6.1 years with an age range 43±66 years. There were eight males and two female. Synchronous SPLC was unilateral in six patients (60%). The mean duration of follow up after operation in synchronous SLPC was 27±13 months.

3.4. Histological classification
Squamous cell carcinoma was the most common histological type, making up to 32 (64%) of the first tumour and 24 (48%) of SLPC (Table 2). Adenocarcinoma, occurred in 14 (27%) of primary lung cancer and in 15 (30%) of SLPC. The histology of the SPLC was different from that of the primary tumour in 23 patients (45%). Fourteen of these had an initial squamous cell carcinoma followed by adenocarcinoma; nine had an initial adenocarcinoma followed by squamous cell carcinoma. Every case whose interval was less than 2 years had a histologically different tumour.

The patient who developed a third metachronous lung tumour had a squamous cell carcinoma for the primary and second cancers followed by carcinoid tumour for the third tumour.

3.5. Pathological staging
The initial metachronous tumour staging was Stage I in 24 patients (60%),Stage II in15 patients (35%) and Stage IIIa in two patients (5%). No primary tumour was more advanced than Stage IIIA.

The second metachronous tumour was in Stage I in 20 patients (48%), Stage II in 13 patients (32%) and Stage IIIa in eight patients (20%). Table 3 shows the stage classification of the primary and second metachronous cancer and the stage of SPLC with respect to that of the initial cancer.

3.6. Management and surgical resection
Patients with metachronous SPLC resection, had their primary tumour treated by lobectomy in 32 patients, pneumonectomy in one patients and segmentectomy in eight patients. The metachronous SPLC were treated by lobectomy in 26, completion pneumonectomy in 11, and wedge/segmental resection in two patients. Radiation therapy was used for treatment of two metachronous SPLC patients who had had a previous pneumonectomy (one patient) or was unfit for surgical intervention (one patient).

Three of the six patients with unilateral synchronous SLPC were treated by pneumonectomy, while the other three unilateral patients were offered radiation therapy, as they were unfit for surgery.

Two of the four patients with bilateral synchronous SLPC were offered staged thoracotomies (initially by lobectomy followed by contralateral lobectomy) performed at 4 and 5 weeks apart, while one patient was treated median sternotomy (lobectomy in one side and wedge resection in the other side). One patient with bilateral synchronous SPLC was unfit for surgical intervention and was treated by palliative radiotherapy (Table 4).

There were no significant difference in risk of development SPLC between segment resection and lobectomy (P=0.09). The risk after pneumonectomy was, however significantly lower than lobectomy or wedge/segment resection (P=0.02).

3.7. Outcome and survival
Eighteen of the 41 patients (43%) with metachronous SLP were alive at the end of the review period. Seventeen were free of cancer while the remaining one patient with Stage IIIA disease was receiving adjuvant radiation therapy for recurrent disease. Twenty patients died within two to 115 months (median 44 months; mean±SD, 46.5±15.4 months) of the second operation. 11 patients died of recurrence (two after wedge and nine after lobectomy), and five died of extra-pulmonary cancers (three colon; one kidney; one oesophagus). Four patients died free of recurrent cancer at the time of death (myocardial infarction three and cerebrovascular accident one). The remaining three patients died in the peri-operative period (two patients died of ARDS and one patient died of myocardial infarction).

Two of the ten patients with synchronous SPLC were alive at the end of the review period. Four of the ten patients (40%) with synchronous SLPC who were treated by radiotherapy died within a period 2–9 months after diagnosis. Two of the remaining six patients with synchronous SPLC died with recurrence, two died of progressive emphysematous chest disease but were free of cancer at the time of death. There was no peri-operative death among the six surgically treated synchronous SPLC.

The overall actuarial 5-year survival for all patients with SPLC was 38% with a median survival of 40 months (range 1–142 months). The actuarial 5-year survival for metachronous SPLC was 44%, median survival of 49 months (range 1–142 months), while the actuarial 5-years survival for synchronous SLPC was 10% with a median survival of 31 months (range 4–78 months). The actuarial 5-year survival rates for metachronous SPLC calculated on the basis of stage of the disease, for Stage I was 49% (median 59 months; range, 1–142 months) while that for Stage II was only 30% (median, 39 months; range, 2–85 months) (P=0.03) (Fig. 2) .

View larger version (12K): [in this window] [in a new window]   Fig. 2. Actuarial 5-year survival of metachronous SPLC compared with that of synchronous SPLC.

View larger version (12K): [in this window] [in a new window]   Fig. 3. Actuarial 5-year survival of Stage I compared with Stage II following operation for metachronous SPLC.

View larger version (13K): [in this window] [in a new window]   Fig. 4. Actuarial 5-year survival of SPLC operated on with the same histology and those with a different histology.

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusions References

Clinically, it is difficult to distinguish a second primary carcinoma from a recurrent or metastatic lesion arising from the first tumour. Martini and Melamed [4] in 1975 outlined very clear criteria for differentiation between the two, which have been used by most subsequent authors, including us. Pairolero and associates [9] using these criteria, reported a 52% 2 years survival for metachronous SLPC compared with 23 and 9% 2-year survival for local and distant recurrent disease, respectively. These data confirm that patients with multiple primary tumours have a more favourable prognosis than patients with locally recurrent or metastatic disease. Therefore a high index of suspicion and careful identification of multiple primary lung cancers helps select the best treatment.

The overall incidence of SPLC in our series is similar to that in the literature [4,9–12] as are the histologic pattern, stage and survival figure. Despite the widespread publicity on smoking and lung cancer and our strict anti-smoking policy, it was disturbing to note that all 41 patients with metachronous SPLC were still smoking at the time of diagnosis of SPLC, and 11 continued to smoke after their second operation! Richardson et al. [13] noted fewer smoking-related SLPC in patients who stopped smoking after their curative surgery and emphasised the need for continuous and concerted education of patients on smoking cessation. Our study concurs with the view that continuation of smoking after lung cancer resection increases the risk of a new primary lung cancer irrespective of the stage of the first cancer.

The assessment of patients with SPLC requires careful attention to resectability and fitness for operation. We try to re-stage all such lesions and operate with the intention to cure whenever possible. If a lung saving procedure such as sleeve lobectomy for the first lesion is done and sufficient pulmonary function is preserved, a second radical operation is possible. Restricted lung function may necessitate a more conservative treatment, including wedge resection, chemotherapy, radiotherapy or a combination of these. A curative yet limited extent of resection allowing for maximum preservation of pulmonary function should be of prime consideration. This policy may allow subsequent treatment of the second lesion by operation. Bronchoplasty, including sleeve resection, has been used frequently at our institution not only for patients with limited lung reserve, but also wherever lung function can be preserved without compromising cancer clearance. If the usual criteria of patient selection for lung resection are used a second resection can be performed safely with reasonable operative mortality and morbidity rates.

The surgical option for second SPLC depend on the extent and site of the new disease, the initial surgical procedure, and the patient's pulmonary function reserve. A previous lesser resection gives a wider range of options for treating the SPLC. Whenever a patient can tolerate another lobectomy, this should be the procedure of choice. A completion pneumonectomy may be feasible for an ipsilateral SPLC. In general, limited resection was favoured for a peripherally located SPLC [11,14] Limited resection is thought to increase local recurrence slightly as shown by Dr Joel Cooper in a multi centric trial, but do not predispose to higher rates of SPLC compared with formal lobectomy. Pneumonectomy was found to decrease the chance of an SPLC significantly; presumably by eliminating ipsilateral metachronous lesions, which otherwise account for about half of the incidence [17].

The poorer survival of synchronous SPLC compared with metachronous lesions has also been reported by others [15–21]. Nevertheless a careful look-out for these second tumours will improve management of these patients. The observation that 70% of synchronous SPLC were discovered preoperatively and 30% intra-operatively should encourage a careful search for SLPC lesions before and during the procedure for primary lung cancer. Others [22,23] have also shown that survival improves as the interval between the primary and metachronous tumour increases. The reduced survival rate of synchronous SPLC compared with single primary cancers might be related to under-staging because of technical difficulties and to tendency for resorting to lesser resections. Further, a significant proportion (40%) of these synchronous SPLCs overall were unfit for anything more than biopsy. Survival rate, however, after SPLC still remain higher than those reported after recurrence [23].

The introduction of chest computed tomography in 1983 increased the awareness of SPLC as an entity. A more aggressive attitude toward any change in symptomatology, radiology, or cytology during follow up has also helped. The mainstay of diagnosis of metachronous SPLC is careful follow up of patients after cancer resection surgery [24,25] and early diagnosis should improve overall survival. As a result of our follow up policy 20 of the 41 (50%) metachronous SPLC were discovered in Stage I. Survival for patients with early stage second primary tumours was significantly better than those with advanced tumour. Diagnosis of a second primary tumour should be followed by the same precise staging investigations and an aggressive therapeutic approach as after any first lung tumour.

	5. Conclusions

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusions References

 
We conclude that SPLC is not infrequent in long-term survivors after curative resection. A high level of awareness and the use of CT scanning helps their early detection. Conservation of lung tissue without compromising cancer clearance during the first resection increases therapeutic options for the second tumour. Follow up after lung resection should be for life and any new development should be carefully investigated to separate a new primary from the more common local recurrence or metastasis. Results of surgical treatment of SPLC are very gratifying and worth the extra effort needed to diagnose and assess these patients.

	Footnotes

 
Presented at the 8th European Conference on General Thoracic Surgery of the European Society of Thoracic Surgeons, London, UK, November 1–4, 2000.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusions References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Tarek M. Aziz Rasheed A. Saad Dhruva Prakash Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Aziz, T. M. Articles by Prakash, D. Search for Related Content PubMed PubMed Citation Articles by Aziz, T. M. Articles by Prakash, D. Related Collections Lung - cancer