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Ann Thorac Surg 2004;78:1194-1199
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Surgical Treatments for Multiple Primary Adenocarcinoma of the Lung

Masao Nakata, MDa,b,*, Shigeki Sawada, MDa, Motohiro Yamashita, MDa, Hideyuki Saeki, MDa,c, Akira Kurita, MDa, Shigemitsu Takashima, MDa, Kazuo Tanemoto, MDb

a Department of Surgery, National Shikoku Cancer Center, Ehime, Japan
b Division of Thoracic and Cardiovascular Surgery, Department of Surgery, Kawasaki Medical School, Okayama, Japan
c Department of Surgery, Sumitomo Besshi Hospital, Ehime, Japan

Accepted for publication March 25, 2004.

* Address reprint requests to Dr Nakata, Division of Thoracic and Cardiovascular Surgery, Department of Surgery, Kawasaki Medical School, Matsushima 577, Kurashiki, Okayama 701-0192, Japan
mnakata{at}med.kawasaki-m.ac.jp


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: The aim of this study was to identify the clinical characteristics of multiple primary adenocarcinomas and to evaluate the efficacy of surgical treatments.

METHODS: Three-hundred sixty-nine patients who underwent pulmonary resection for adenocarcinoma from January 1994 to December 2002 were reviewed.

RESULTS: Thirty-one patients (8.4%) were determined to have multiple primary adenocarcinomas that could be detected on chest x-rays or computed tomography (CT). Twenty-six patients were synchronous and five patients were metachronous with a median interval of 59.0 months. Forty-nine (72.1%) of the total 68 lesions exhibited ground-glass opacity on high-resolution CT (HRCT). Pathologically well-differentiated adenocarcinoma with mixed bronchioloalveolar pattern was the most common subtype (39.7%). Taking into consideration pulmonary function, size, location, and HRCT findings of the lesions the procedures performed were lobectomy with mediastinal lymph-node dissection for 32 patients, segmentectomy with hilar node dissection for 8 patients, and wedge resection for 28 patients. Of 17 patients with bilateral synchronous cancers, simultaneous bilateral pulmonary resection was performed in 14 patients including simultaneous bilateral video-assisted thoracic surgery (VATS) in 11 patients. After a median follow-up period of 27.7 months, the 3-year overall survival rate was 92.9% and the 3-year disease-free survival rates of synchronous cancer and metachronous cancer were 77.9% and 100%, respectively.

CONCLUSIONS: The incidence of multiple primary adenocarcinomas was relatively common. Early radiographic detection and surgical excision could yield a favorable prognosis. The use of VATS, even for synchronous bilateral patients, was a safe and beneficial procedure.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Adenocarcinoma is the most common type of lung cancer according to the recently reported series. With the widespread use of low-dose helical computed tomography (CT) for lung cancer screening, a noted increase in the detection of small adenocarcinoma in the periphery has been documented [1–3]. A majority of CT-detected adenocarcinomas exhibit a mixed bronchioloalveolar pattern that is thought to develop through atypical adenomatous hyperplasia (AAH)-carcinoma multistep sequences [4]. Several microscopic studies on surgical specimens have already reported the multicentricity of these replacement-type adenocarcinomas [5–7]. Although these pathologic studies have provided considerable insight into the carcinogenesis of pulmonary adenocarcinomas, these tiny lesions sustained little impact on the decision making regarding treatment, because they could rarely be preoperatively identified on conventional chest x-rays. However with the recent advances in high-resolution CT (HRCT) imaging, increased detection of multiple primary adenocarcinomas at the clinical level has resulted in a strong interest and controversies regarding the diagnosis and management of these lesions. Although several previous studies have reported successful resection for multiple lung cancers [8–11], appropriate treatment strategies and postsurgical outcomes remain controversial. Because the resection of multicentric lesions exhibits some limitations with regard to pulmonary reserve, the adequate candidates for limited resection and the prognostic factors must be clarified. In this study we reviewed our surgically resected instances of multiple primary adenocarcinomas to identify the clinical characteristics of these lesions and to evaluate the efficacy of surgical treatments.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
From January 1994 to December 2002, 517 patients underwent pulmonary resection for non-small cell lung cancer at the National Shikoku Cancer Center (Ehime, Japan). All patients underwent preoperative examinations including plain chest roentgenogram, HRCT of the chest, ultrasonography of the upper abdomen, magnetic resonance imaging of the brain, and bone scintigraphy. There were 369 patients with adenocarcinoma, 111 with squamous cell carcinoma, 19 with adenosquamous carcinoma, 15 with large cell carcinoma, and 3 with other types of carcinoma. According to the criteria proposed by Martini and Melamed [12] (Table 1), 41 (7.9%) out of 517 patients were determined to exhibit multiple primary lung cancers. For the evaluation of the efficacy of the surgical treatments, multiple lesions identified only by postsurgical microscopic examination were excluded. Thirty-five patients exhibited the same histologic types of multiple lung cancers (31 adenocarcinomas and 4 squamous cell carcinomas) and 6 patients exhibited different histologic cell types. In this study 31 patients with multiple primary adenocarcinomas were retrospectively studied. For the radiologic review, we classified all the multiple lesions into three categories according to the area of ground-glass opacity (GGO) on HRCT images: pure GGO that consisted of almost 100% homogeneous translucent density (Fig 1) , mixed GGO that consisted of GGO for more than 50% of the lesion (Fig 2) , and solid lesion that consisted of GGO for less than 50% of the lesion (Fig 3). Histologic diagnoses were assessed according to the revised World Health Organization histologic classification [13]. Patients were followed up with a chest roentgenogram at the outpatient clinic at least every 6 months and also with annual CT scans. Survival time was calculated from the date of first surgery for synchronous multiple patients and from the date of second surgery for metachronous multiple patients. Cumulative survival rates were calculated by the Kaplan–Meier method.


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  		Table 1. Criteria for Diagnosis of Primary Lung Cancers of Similar Histology According to Martini and Melamed [12]

 


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  		Fig 1. Pure ground-glass opacity that consisted of almost 100% homogeneous translucent density.

 


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  		Fig 2. Mixed ground-glass opacity (GGO) that consisted of GGO for more than 50% of the lesion.

 


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  		Fig 3. Solid lesion that consisted of ground-glass opacity for less than 50% of the lesion.

 

   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Thirty-one patients exhibited primary multiple adenocarcinomas; that corresponded to 8.4% of the total 369 adenocarcinoma patients who underwent surgical resection during the same period. There were 12 males and 19 females with a median age of 68.1 years (range, 47–81). Thirteen patients (41.9%, 11 male and 2 female) exhibited a history of smoking. The incidence of primary multiple adenocarcinomas was substantially higher in female and nonsmokers than that of other histologic multiple lung cancers (Table 2). Twenty-six patients were synchronous and 5 patients were metachronous. The median interval between the two adenocarcinomas in the metachronous instances was 59.0 months (range, 26–146). There were 26 patients with double primary cancer, 4 patients with triple cancer, and 1 patient with quadruple cancer. Of the total 68 lesions, 30 lesions (44.1%) were detectable on a chest roentgenogram, whereas the remaining 38 lesions (55.9%) were detectable only on helical CT images. Of the 26 patients with synchronous multiple adenocarcinomas, 9 patients exhibited unilateral multiple lesions and 17 patients exhibited bilateral lesions. With regard to the HRCT image, 20 lesions were classified as pure GGO, 29 as mixed GGO, and 19 as solid lesions. The mean diameter of the lesions in each group was 12.4, 23.4, and 21.8 mm, respectively.


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  		Table 2. Characteristics of Patients With Multiple Primary Lung Cancer

 
Surgical procedures were selected based on performance status and pulmonary function as well as the size, location, and HRCT findings of the lesions. Based on our previous study [14], pure GGO lesions were intended for limited resection. Performed procedures included lobectomy with systemic lymph-node dissection for 32 lesions (including 10 lesions existing in the same lobe), segmentectomy with hilar node dissection for 8 lesions, and wedge resection for 28 lesions (Table 3). Lobectomy was performed in 7 of the 20 pure GGO lesions because of the existence of another lesion in the same lobe. Wedge resection was performed in the other 13 patients. For the 29 mixed GGOs and 19 solid lesions, the procedures were indicated as follows: lobectomy was performed in 25 patients, segmentectomy was performed in 8 patients, and wedge resection was performed in 15 patients. In the 5 metachronous patients, lobectomy was performed for the first adenocarcinoma and all patients were pathologically diagnosed as stage I. Procedures for the second tumor included wedge resection in 4 patients and segmentectomy in 1 patient. Of the 17 patients with bilateral synchronous cancers, simultaneous bilateral pulmonary resection was performed in 14 patients including 4 triple and 1 quadruple cancer. The surgical approaches in these 14 patients included simultaneous bilateral video-assisted thoracic surgery (VATS) in 11 patients and muscle-sparing thoracotomy for the other 3 patients. The surgical procedures performed by simultaneous bilateral VATS constituted lobectomy in 6 patients, segmentectomy in 5 patients, and wedge resection in 14 patients.


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  		Table 3. Surgical Procedure

 
The histologic diagnoses of the 68 lesions identified as well-differentiated (W/D) adenocarcinoma with mixed bronchioloalveolar pattern in 27 of them, moderately differentiated (M/D) adenocarcinoma in 17, poorly differentiated (P/D) adenocarcinoma in 3, and bronchioloalveolar carcinoma (BAC) in 21 (Table 4). Of the 20 pure GGO lesions, 15 were diagnosed as BAC and 5 were diagnosed as W/D adenocarcinoma. No lymphatic infiltrations were identified in any of the pure GGO lesions. Of the 29 mixed GGO lesions, 6 were diagnosed as BAC, 16 were diagnosed as W/D adenocarcinoma, and 7 were diagnosed as M/D adenocarcinoma. Six of the 29 lesions (20.7%) exhibited lymphatic infiltration and 1 patient exhibited ipsilateral mediastinal lymph-node metastasis (N2 disease). The histologic diagnoses of the 19 solid lesions depicted W/D adenocarcinoma in 6 of them, M/D adenocarcinoma in 10 of them, and P/D adenocarcinoma in 3 of them. Eleven of the 19 lesions (57.9%) exhibited lymphatic infiltrations and 1 patient exhibited N2 disease. The pathologic stages of the 68 lesions were classified as IA in 54, IB in 12, and IIIA in 2.


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  		Table 4. Pathological Diagnoses of Multiple Primary Adenocarcinoma

 
One patient who underwent lobectomy for unilateral synchronous cancers expired because of pulmonary embolism on the fifth postoperative day. Except for this patient, there were no major postoperative complications even after the simultaneous bilateral VATS procedure. After a median follow-up period of 27.7 months, the 3-year overall survival rate was 92.9% and the 3-year disease-free survival rate was 81.1% (Fig 4). The 3-year disease-free survival rates with synchronous cancer and metachronous cancer were 77.9% and 100%, respectively. The relapse sites were distant in 2 patients with IB and IIIA disease and local relapse occurred in the surgical stump after wedge resection for a solid lesion in 1 patient.



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  		Fig 4. Survival curves for patients with primary multiple adenocarcinomas. The 3-year overall survival rate was 92.9% and the 3-year disease-free survival rate was 81.1%.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
In our retrospective study, 7.9% of surgically resected non-small cell lung cancers and 8.4% of adenocarcinomas exhibited multiple lesions. The incidence of multiple primary lung cancer in our study was comparable with that in previous studies that reported an incidence of 1%–10% [9, 15, 16]. However a higher incidence of multiple synchronous adenocarcinomas was a marked characteristic of our series compared with previous reports [8, 10, 17, 18]. Even if our study exhibits a limitation of a short follow-up period, it should be noted that multiple synchronous adenocarcinomas constituted the majority (26 out of 41) of multiple primary lung cancer instances. One of the reasons for the increasing incidence of multiple adenocarcinomas would be the widespread use of low-dose helical CT screening. Several studies have already reported a notably increased detection of small peripheral adenocarcinoma by CT screening [1–3]. In addition, the recent advances in CT resolution could have contributed to the detection of small hazy lesions. Fifty-six percent (38 out of 68) of the lesions analyzed in our study could only be detected on CT images and not on conventional chest X-rays. Forty-nine lesions (72.1%) revealed GGO on HRCT images and 48 lesions (70.6%) exhibited a bronchioloalveolar growth pattern histologically including 21 instances of non-mucinous BAC. These results indicate that the incidence of multiple adenocarcinomas is relatively common, and that adenocarcinoma with a bronchioloalveolar growth pattern indicates a multifocal feature. Therefore, a detailed radiologic study would be necessary for patients exhibiting pulmonary adenocarcinoma, especially those with a GGO appearance in consideration of the high incidence of multiple lesions. Our patient characteristics also differed with the histologic shift of multiple lung cancer. In contrast to the dominance of male smokers in the older series [18, 19] and our patients with other histologic multiple lung cancer, 61.3% (19 out of 31) of our patients were female and 58.1% (18 out of 31) were nonsmokers. Japanese studies on helical CT screening have also reported a high prevalence of peripheral pulmonary adenocarcinoma in nonsmoking females [1–3]. These data suggest that the definition of the "high-risk" population for lung cancer screening should be reconsidered so as not to overlook the increasing incidence of adenocarcinoma in nonsmoking females.

Several previous studies have reported the successful surgical resection of multiple lung cancers [9, 11, 19]. However, critical limitations with regard to pulmonary reserve are often encountered in surgical treatment. Although The Lung Cancer Study Group demonstrated a higher incidence of locoregional recurrence after limited resection than after lobectomy [20], limited resection is inevitable for patients with multiple primary lung cancer only because of the number, size, and location of the lesions. However, the adequate candidates for limited pulmonary resection still remain controversial. Although Okada and associates [21] indicated an equivalent survival rate after extended segmentectomy compared with standard lobectomy for patients with lung cancer lesions of 2 cm or less, wedge resection has not been accepted as an alternative procedure for primary lung cancer. We previously reported successful results of thoracoscopic wedge resection for pure GGO lesions selected on the HRCT images [14]. Based on our criteria, we performed wedge resection for 13 out of 20 patients with pure GGO lesions, and pathologic examinations revealed that 15 out of those 20 patients with lesions indicated noninvasive BAC and none of the lesions exhibited lymphatic infiltration. In contrast, 20.7% (6 out of 29) of the mixed GGO lesions and 57.9% (11 out of 19) of the solid lesions exhibited lymphatic infiltration. Although local recurrence along the surgical stump was identified in 1 patient who underwent limited resection for a solid lesion because of poor pulmonary reserve, there has been no recurrence to date in patients with pure GGO lesions. We believe that the area of GGO on HRCT images could be a useful criterion for selecting surgical procedures with regard to adenocarcinoma, and that wedge resection could be valid for pure GGO lesions.

The timing of surgical resection for bilateral synchronous multiple lung cancer is also controversial. In previous reports, staged bilateral thoracotomies were often adopted with an interval of several weeks [19]. However, staged resection might bring on considerable physical strain and there could even be a risk of interval progression of the disease. Although adenocarcinoma with a bronchioloalveolar growth pattern exhibits a slow-growing feature [22], lymphatic infiltration and lymph-node involvement were identified in mixed GGO lesions. Therefore, simultaneous pulmonary resection should be recommended from an oncologic viewpoint. We performed simultaneous bilateral resection for 14 out of 17 patients with bilateral synchronous multiple adenocarcinomas. Until recently, median sternotomy has been widely used for bilateral pulmonary resection, although there are some difficulties regarding lower pulmonary resection with this approach. On the other hand, the bilateral VATS approach that we employed for 11 patients could yield a wide view of the intrathoracic structure and minimal destruction of the thoracic wall. There were no postoperative complications in any of these 11 patients. Regarding the curability of malignant disease with the VATS procedure, a favorable survival rate after VATS lobectomy for lung cancer patients has already been reported in several early studies [23, 24]. We believe that the bilateral simultaneous VATS approach is a safe and useful procedure for patients with multiple primary bilateral adenocarcinomas.

The postsurgical outcome for multiple primary lung cancer has been relatively poor. Specifically the 5-year survival rate for synchronous multiple cancers has been reported to be 0%–44% [8, 10, 18, 19]. Our current results, despite a short follow-up period, indicated 92.9% of the 3-year overall survival rate and 81.1% of the 3-year disease-free survival rate. Even for synchronous patients, the 3-year disease-free survival rate was 77.9%. One of the reasons for our favorable results was the early detection of multiple adenocarcinomas. Because CT-detected GGO lesions are thought to be early adenocarcinoma [25, 26], careful radiologic study for focal GGO lesions on HRCT images would be essential for achieving a successful outcome. Another reason would be the low-grade malignant behavior of replacement-type adenocarcinoma. Aoki and associates [22] reported that 83% of bronchioloalveolar carcinoma detected as focal GGO on HRCT had exhibited a tumor doubling time of more than 1 year. With regard to this point our results are quite primitive for assessing the outcome of slow-growing tumors because of a short follow-up period. However, in terms of treating such a slow-growing malignancy, minimal invasiveness is required for an improved postoperative quality of life. In that sense, our surgical strategies that involve the use of VATS or wedge resection are thought to be beneficial and valid.

In conclusion, the incidence of multiple primary adenocarcinoma in the candidates for surgical treatment is relatively common. Histologically, 70% of lesions are W/D adenocarcinoma with a bronchioloalveolar growth pattern. Careful radiologic study of synchronous GGO lesions is necessary for the early detection of multiple adenocarcinoma, which is associated with a favorable outcome. The simultaneous bilateral VATS approach is safe and useful for selected patients with early synchronous multiple adenocarcinomas.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Kaneko M, Eguchi K, Ohmatsu H, et al. Peripheral lung cancer: screening and detection with low-dose spiral CT versus radiography. Radiology. 1996;201:798–802[Abstract/Free Full Text]
  2. Sone S, Takashima S, Li F, et al. Mass screening for lung cancer with mobile spiral computed tomography scanner. Lancet. 1998;351:1242–1245[Medline]
  3. Sobue T, Moriyama N, Kaneko M, et al. Screening for lung cancer with low-dose helical computed tomography: Anti-lung cancer association project. J Clin Oncol. 2002;20:911–920[Abstract/Free Full Text]
  4. Noguchi M, Morikawa A, Kawasaki M, et al. Small adenocarcinoma of the lung. Histologic characteristics and prognosis. Cancer. 1995;75:2844–2852[Medline]
  5. Zwirewich CV, Miller RR, Muller NL. Multicentric adenocarcinoma of the lung: CT-pathologic correlation. Radiology. 1990;176:185–190[Abstract/Free Full Text]
  6. Suzuki K, Takahashi K, Yoshida J, et al. Synchronous double primary lung carcinomas associated with multiple atypical adenomatous hyperplasia. Lung Cancer. 1998;19:131–139[Medline]
  7. Koga T, Hashimoto S, Sugio K, et al. Lung adenocarcinoma with bronchioloalveolar carcinoma component is frequently associated with foci of high-grade atypical adenomatous hyperplasia. Am J Clin Pathol. 2002;117:464–470[Medline]
  8. Rosengart TK, Martini N, Ghosn P, et al. Multiple primary lung carcinomas: prognosis and treatment. Ann Thorac Surg. 1991;52:773–778[Abstract]
  9. Okada M, Tsubota N, Yoshimura M, et al. Operative approach for multiple primary lung carcinomas. J Thorac Cardiovasc Surg. 1998;115:836–840[Abstract/Free Full Text]
  10. Rea F, Zuin A, Callegaro D, et al. Surgical results for multiple primary lung cancers. Eur J Cardiothorac Surg. 2001;20:489–495[Abstract/Free Full Text]
  11. Battafarano RJ, Meyers BF, Guthrie TJ, et al. Surgical resection of multifocal non-small cell lung cancer is associated with prolonged survival. Ann Thorac Surg. 2002;74:988–994[Abstract/Free Full Text]
  12. Martini N, Melamed MR. Multiple primary lung cancers. J Thorac Cardiovasc Surg. 1975;70:606–612[Abstract]
  13. Travis WD, Colby TV, Corrin B, et al. Histological typing of lung and pleural tumours (World Health Organization International Histological Classification of Tumors). 3rd ed. Berlin: Springer; 1999. p. 25–47
  14. Nakata M, Sawada S, Saeki H, et al. Prospective study of thoracoscopic limited resection for ground-glass opacity selected by computed tomography. Ann Thorac Surg. 2003;75:1601–1606[Abstract/Free Full Text]
  15. Shields TW, Humphrey EW, Higgins GA, et al. Long-term survivors after resection of lung carcinoma. J Thorac Cardiovasc Surg. 1978;76:439–445[Medline]
  16. Van Bodegam PC, Wagenaar SS, Corrin B, et al. Second primary lung cancer: importance of long term follow up. Thorax. 1989;44:788–793[Abstract/Free Full Text]
  17. Verhagen AF, Tavilla G, van de Wal HJ, et al. Multiple primary lung cancers. Thorac Cardiovasc Surg. 1994;42:40–44[Medline]
  18. Ribet M, Dambron P. Multiple primary lung cancers. Eur J Cardiothorac Surg. 1995;9:231–236[Abstract]
  19. Adebonojo SA, Morits DM, Danby CA. The results of modern surgical therapy for multiple primary lung cancers. Chest. 1997;112:693–701[Abstract/Free Full Text]
  20. Lung Cancer Study Group. Randomized trial of lobectomy versus limited resection for T1N0 non-small cell lung cancer. Ann Thorac Surg. 1995;60:615–623[Abstract/Free Full Text]
  21. Okada M, Yoshikawa K, Hatta T, et al. Is segmentectomy with lymph node assessment an alternative to lobectomy for non–small cell lung cancer of 2 cm or smaller? Ann Thorac Surg. 2001;71:956–960[Abstract/Free Full Text]
  22. Aoki T, Nakata H, Watanabe H, et al. Evolution of peripheral lung adenocarcinomas: CT findings correlated with histology and tumor doubling time. Am J Roentgenol. 2000;174:1743–1763
  23. Kaseda S, Aoki T, Hangai N, et al. Better pulmonary function and prognosis with video-assisted thoracic surgery than with thoracotomy. Ann Thorac Surg. 2000;70:1644–1646[Abstract/Free Full Text]
  24. Gharagozloo F, Tempesta B, Margolis M, et al. Video-assisted thoracic surgery lobectomy for stage I lung cancer. Ann Thorac Surg. 2003;76:1009–1015[Abstract/Free Full Text]
  25. Nakata M, Saeki H, Takata I, et al. Focal ground-glass opacity detected by low-dose helical CT. Chest. 2002;121:1464–1467[Abstract/Free Full Text]
  26. Jang HJ, Lee KS, Kwon OJ, et al. Bronchioloalveolar carcinoma: focal area of ground-glass attenuation at thin-section CT as an early sign. Radiology. 1996;199:485–488[Abstract/Free Full Text]



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