Ann Thorac Surg 2004;78:1011-1016
© 2004 The Society of Thoracic Surgeons
Original article: general thoracic
A clinicopathological study of resected adenocarcinoma 2 cm or less in diameter
Norihiko Ikeda, MD, PhDa,*,
Junichi Maeda, MDa,
Koichi Yashima, MDa,
Masahiro Tsuboi, MDa,
Harubumi Kato, MD, PhDa,
Soichi Akada, MD, PhDb,
Shinya Okada, MD, PhDc
a Department of Thoracic Surgery, Tokyo Medical University, Tokyo, Japan
b Department of Radiology, Tokyo Medical University, Tokyo, Japan
c Department of Pathology, Tokyo Medical University, Tokyo, Japan
Accepted for publication March 15, 2004.
* Address reprint requests to Dr Ikeda, 6-7-1, Nishishinjuku, Shinjuku-ku, Tokyo 160-0023, Japan
ikeda{at}wd5.so-net.ne.jp
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Abstract
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BACKGROUND: The biological behavior of small adenocarcinoma is different in each patient and these are especially enormous differences when evaluating solid tumors and nonsolid tumors.
METHODS: A total of 159 adenocarcinomas 2 cm or less in diameter were studied. Several clinicopathological factors were retrospectively analyzed.
RESULTS: The diameter of the primary tumors was less than 1 cm in 47 patients, 1–1.5 cm in 49 patients, and 1.5–2 cm in 63 patients, respectively. Almost all patients (147) were pathologic N0 and there were 12 node-positive patients (7.5%). Lymph-node involvement was observed in 1 patient with a tumor diameter measuring less than 1 cm and in 11 patients with a tumor diameter measuring 1–2 cm. According to Noguchi' s classification, 33 patients belonged to class A or B, 71 patients belonged to class C, and 55 patients belonged to class D, E, or F. The ratio of ground-glass opacity (GGO) area in the main tumor in high resolution computed tomography was classified into two groups with a threshold of 50%. There were 44 patients with a GGO ratio of equal to or greater than 50%, none of which indicated lymph-node metastasis or tumor recurrence during follow-up (5-year survival = 100%). On the contrary among 115 patients with a GGO ratio less than 50%, lymph-node involvement was indicated in 12 patients (10.4%) and the 5-year survival rate was 83.9%.
CONCLUSIONS: The biological malignancy of small adenocarcinomas might be accurately evaluated by the proportion of GGO area as well as the Noguchi classification.
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Introduction
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Lung cancer is the greatest cause of cancer-related death in the world because most lung cancers are detected at a late stage and curative treatment is not an option. Nevertheless a cure rate of greater than 70% was obtained in completely resected patients of stage I cancer [1]. Prevention and early detection are thus essential with regard to the reduction of lung cancer mortality. Adenocarcinoma is the most common type of lung cancer arising from the peripheral lung parenchyma. Chest x-ray surveys have been considered useful for early detection. However if the lesions are located in a "dead angle" on the chest roentgenogram film, such as behind the aorta or heart, abnormalities may be overlooked. Bronchioloalveolar carcinoma (BAC) seldom reveals abnormalities on chest roentgenogram because it grows without destroying alveolar structure [2]. Helical computed tomography (CT) screening has greatly increased the sensitivity of cancer detection compared with that of conventional chest roentgenogram screening [3–7]. A prospective randomized trial comparing the lung cancer mortality rate of a CT screening group with that of a conventional chest roentgenogram screening group has been conducted by the National Cancer Institute [8]. In this respect, the biggest issue facing thoracic surgeons is the treatment strategy for small cancers detected by CT screening, including the possibility of limited resection. BAC is known to exhibit a relatively nonaggressive nature, therefore a favorable outcome can be expected after curative operation [2, 9–12]. However patients with solid images on chest CT tend to have invasive adenocarcinomas and their survival is definitely worse than that of BAC [9–11]. Pathologic classification of the tumor is essential regarding the evaluation of the aggressiveness of each patient [2] but postoperative pathologic findings cannot exhibit a strong impact on the choice of treatment.
There are several reports indicating that the ratio of the size of ground-glass opacity (GGO) and that of consolidation on high resolution CT (HRCT) is strongly related to the stage and prognosis of the cancer [10, 13–15]. Lung cancers with a large GGO component tend to be BAC or minimally invasive adenocarcinomas that exhibit favorable prognoses [10, 13–15]. If a definition of peripheral early cancer could be established, it would be useful with regard to selecting optimal treatment for individual patients. For this purpose we retrospectively analyzed clinicopathological features of adenocarcinomas with a diameter of 2 cm or less resected in our hospital between 1997–2002.
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Patients and methods
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Patients
A total of 983 lung cancer operations were performed from January 1997 to December 2002 at the Department of Thoracic Surgery, Tokyo Medical University Hospital (Tokyo, Japan). Among these, there were 168 patients with peripheral adenocarcinomas less than 2 cm in diameter as well as a total of 159 patients who had undergone high-resolution computed tomography (HRCT) and in whom complete records were available for study (Table 1). There were 67 men and 92 women ranging in age from 40–84. There were 89 nonsmokers and 70 smokers. The primary lesions were detected by chest x-ray in 115 patients: detection was determined by mass survey or private general check-up in 81 patients, follow-up for other diseases in 18 patients, and respiratory symptoms in 16 patients. The other 44 patient's lesions were detected by chest CT performed by mass survey program or private general check-up.
All patients underwent a physical examination and blood examination, respiratory function test, electrocardiogram, and chest radiography. Also, all patients received helical CT of the chest preoperatively with 10-mm thick continuous sections. HRCT images with 1–2 mm slices of the primary tumors were then performed to obtain the precise findings of GGO and consolidation of the tumors. Histologic typing was diagnosed based upon the classification of the World Health Organization (WHO) and we also classified all of the patients into six subtypes using the Noguchi classification. The staging of patients was determined by the thoracic wall, node involvement, and metastases (TNM) classification of the International Union Against Cancer (UICC).
Lobectomy combined with systemic mediastinal lymph-node dissection was performed in 112 patients and limited surgery was performed in 47 patients. Of these 47 patients, 37 received intentionally limited operation because of the nonaggressive appearance on HRCT and the remaining 10 patients because of impaired condition. Segmentectomy with mediastinal sampling was performed in 27 patients and wedge resection without nodal dissection was performed in 20 patients. All patients that underwent wedge resection indicated pure GGO or enormously GGO-dominant findings on HRCT as well as being clinically node negative.
CT findings
In this study the ratio of the size of solid attenuation to that of GGO was extensively analyzed. GGO was defined as a hazy increase in lung attenuation without obscuration of the underlying vascular marking. At least two experienced chest surgeons and radiologists reviewed the hard-copy films of HRCT and determined the maximal area of GGO and tumor. Discrepancies between reviewers were resolved by consensus. The ratio area of GGO to the area of primary tumor was calculated as illustrated in Figure 1. Patients were divided into two groups: those with a GGO ratio greater than 50% and those with a GGO ratio less than 50%.
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Fig 1. Thin section computed tomographic scan of lung cancer depicting solid attenuation and ground-glass opacity (GGO). The largest area of tumor (solid line) and solid attenuation (dotted line) were decided based on this film. The proportion of GGO area to the entire tumor was defined; GGO ratio = (maximum GGO – maximum consolidation)/maximum GGO. Max GGO (solid arrow); Max consolidation (dotted arrow).
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Pathology
Resected lungs were fixed in formalin and stained by hematoxylin and eosin staining in a routine manner and also stained with elastica van Gieson. Experienced pathologists diagnosed the subtypes of primary tumors according to the Noguchi classification as well as the nodal status. The Noguchi classification is presented in Table 2. Types A and B are considered to be noninvasive cancers and types D, E, and F are considered to be invasive cancer.
Statistics
We examined the relation of the proportion of GGO area to maximal tumor size, stage, Noguchi classification, and other prognostic factors. The 
2 test using StatView 5.0 (SAS Institute Inc., Cary, NC) was performed and the differences were considered to be statistically significant when the p value was less than 0.05. All patients were periodically examined and the average length of follow-up was 40 months. The 5-year survival curve was obtained using the Kaplan–Meier method.
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Results
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A total of 159 patients were studied. The size was classified into three categories: 1 cm or less, 1–1.5 cm, and 1.5–2 cm. There were 47, 49, and 63 patients, respectively. There were 147 pathologic N0 patients and lymph-node metastasis was recognized in 12 patients (7.5%); N1 in 3 patients and N2 in 9 patients. Table 3 lists the rate of lymph-node involvement according to tumor size. Lymph-node involvement was not indicated in 98% of patients who had a tumor size of 1 cm or less, however even in patients with tiny tumors, 2% indicated N2 disease. In patients who had a tumor size of 1 and 1.5 cm, 94% indicated no metastasis but 6% were either N1 or N2. In patients who had a tumor size of 1.5 and 2 cm, lymph-node involvement was recognized in 13%.
In this study the proportion of the size of GGO to that of the tumor was extensively analyzed. We divided patients into two categories according to how much of the lesion consisted of GGO findings. According to these criteria, 44 tumors consisted of greater than 50% of GGO and 115 tumors consisted of less than 50% of GGO. Patients with a GGO ratio of greater than 50% indicated no lymph-node metastases. On the contrary all node-positive patients indicated a GGO ratio of less than 50% (Table 3). The relationship between the proportion of GGO area on HRCT and the Noguchi classification is indicated in Table 4.
Twenty-five out of 44 patients (76%) of types A and B indicated a GGO component of greater than 50% on HRCT. Seventeen out of 71 patients (24%) of type C indicated greater than 50% GGO and the remaining 54 patients (76%) indicated less than 50% GGO. Fifty three out of 55 patients (96%) of types D, E, and F tumors indicated less than 50% GGO. A favorable correlation between CT findings and the Noguchi classification was recognized.
The relationship between representative clinicopathological factors and the proportion of GGO area is indicated in Table 5. According to the 2 test, the ratio of GGO area to that of the tumor is related to the tumor size (p = 0.0135) and pathologic stage (p = 0.04). In particular a significant relationship was obtained regarding the pathologic features including Noguchi classification (p = 0.0001), vascular invasion, and lymphatic invasion .
Patients were followed-up in the outpatient clinic and periodically received blood examinations, chest roentgenogram, and chest CT. The median follow-up period for all patients was 40 months. The overall 5-year survival rate of patients studied was 88.0% (Fig 2), but it was 96.7% in patients with tumors less than 1 cm in diameter, 81.6% in patients with tumors between 1 and 1.5 cm, and 84.4% in patients with tumors between 1.5 and 2 cm (Fig 3).
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Fig 3. Five-year survival rate according to tumor size. Less than or equal to 1 cm = 96.7%, 1.0–1.5 cm = 81.6%, 1.5–2.0 cm = 84.4%.
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The 5-year survival rate according to how much of the lesion consisted of GGO findings was also analyzed. In patients with tumors greater than 50% GGO, a 100% 5-year survival rate was obtained, but in patients with tumors less than 50% GGO an 83.9% 5-year survival rate was obtained (Fig 4)
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Fig 4. Five-year survival rate according to the proportion of ground-glass opacity (GGO) area. A GGO dominant patient indicated a 100% 5-year survival, whereas patients exhibiting a GGO area less than 50% indicated an 83.9% 5-year survival.
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The survival rate according to the Noguchi classification is illustrated in Figure 5. A 100% 5-year survival rate was obtained in types A and B, 97.4% in type C, and 67.1% in types D, E, and F, respectively, which was statistically lower than the results of types A, B, and C.
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Fig 5. Five-year survival rate according to the Noguchi classification. Noguchi A, B indicated a 100% 5-year survival, type C indicated a 97.4% 5-year survival, and types D, E, and F, indicated a 67.1% 5-year survival, respectively.
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Comment
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Because of the increasing widespread application of helical CT, the detected number of small lung peripheral nodules has enormously increased [3–7]. In addition the size of peripheral type adenocarcinomas has been smaller on average when they were detected. This has raised several issues: discerning how to discriminate malignant from benign nodules, the usefulness of CT screening in diminishing lung cancer mortality, the optimal intervention in patients who have small nodules, and so on [16, 17]. The management of small cancers is a particular concern of thoracic surgeons, because some of these small cancers might be managed appropriately by limited resection. As previously reported adenocarcinoma tends to metastasize to the regional lymph nodes even if small in size. Nearly 20% of adenocarcinomas less than 2 cm in diameter were reported to be node positive and 5% of adenocarcinomas less than 1 cm were also considered as N1 or N2 disease [18–20]. The Lung Cancer Study Group failed to demonstrate positive results with regard to limited resection for clinical T1 lung cancers. The limited surgery group indicated a local recurrence rate of 5–6 times higher than the lobectomy group [21]. Thus lobectomy and locoregional lymph-node dissection have been recommended as standard lung cancer procedures. However if peripheral early cancer is properly defined, such patients could be managed by lesser resection, which would be useful with regard to decreasing the operative mortality and morbidity as well as enhancing the performance status of the patients.
In our study 12 out of 159 patients (7.5%) exhibited lymph-node metastasis and even tumors measuring 1 cm or less indicated lymph-node metastasis in 2% of patients. The 5-year survival rate did not indicate a statistically significant difference between the three groups according to tumor size in this study. There are reports that 5%–8% of such tiny adenocarcinomas indicated lymph-node metastasis [18, 22]. Kondo reported 57 adenocarcinomas measuring 1 cm or less, none of which indicated lymph-node metastasis, and 49 revealed BAC without destructive growth that were categorized as nonaggressive tumors [23]. This demonstrates that the indications of limited surgery cannot be determined by size alone. In our study, 47 patients received limited resection. Out of these, mediastinal lymph node or sampling were performed in 20 patients and the rest of 27 patients received wedge resection without nodal dissection. Of these 27 patients stage migration may occur because nodal status was not evaluated pathologically. However these patients indicated pure GGO or overwhelmingly dominant GGO findings on chest CT as well as being clinically node negative. Such patients have been reported to be free from lymph-node metastasis [10, 12–15, 20] and recurrence was not observed in any of these patients by chest CT examination during follow-up. Therefore we classified these patients as N0 in this study. Noguchi classified small adenocarcinomas into six categories (types A–F) and this classification indicated a favorable correlation with the biologically aggressive nature of the tumor [2]. Types A and B are localized BAC with or without foci indicating a collapse of alveolar structures that are recognized to be noninvasive. Types D, E, and F are poorly differentiated, tubular, papillary type, respectively, and are invasive. Pathologic analysis revealed that all type A and B patients were N0, however 25%–56% of type D, E, and F patients indicated lymph-node metastasis [2]. Many thoracic surgeons postulated that certain types of adenocarcinomas might be candidates for limited resection and have sought for criteria of "peripheral early cancer." The Noguchi classification is useful with regard to evaluating the aggressive nature in individual patients, but this criteria is based on postoperative pathologic findings and could not have a strong impact on the choice of treatment. Therefore we require criteria that are available preoperatively to define early minimally invasive cancers.
Increased amounts of collagenization or hyalinization microscopically detected in the central fibrotic focus in adenocarcinoma have been reported to influence the prognosis and the smaller the central fibrosis, the more favorable the prognosis [24, 25]. Suzuki reported that central fibrosis in a tumor corresponds to consolidation on HRCT. Thus the ratio of the area of GGO and that of consolidation seems to be strongly related to nodal status and stage [25].
In our study there were 12 N1 or N2 out of 159 patients, in all of whom the proportion of the area of GGO to the entire tumor was less than 50%. All patients with a ratio of GGO greater than 50% survived without recurrence during the follow-up period, although patients with GGO less than 50% indicated an 83.9% 5-year survival rate. The proportion of the GGO area correlates well with the Noguchi classification [26]. There were 33 Noguchi type A and B patients, 25 of which indicated a GGO area of greater than 50% and 8, of which indicated a GGO area of less than 50%. As for type D, E, and F patients, 53 out of 55 indicated a low GGO% and only 2 patients belonged to the high GGO ratio group. A statistically significant correlation was obtained between GGO% and Noguchi classification but types A and B could be completely diagnosed by HRCT findings as they should be the suitable indication of limited surgery. The 5-year survival rate of the high GGO group was 100% and the 5-year survival rate of the low GGO group was 83.9%. Similar results were obtained by Matsuguma who compared the preoperative HRCT findings with pathologic results in 96 patients who underwent surgical resection because of stage Ia cancers [14]. They determined that patients in whom the proportion of GGO to the whole tumor on CT was equal to or greater than 50% exhibited no nodal metastasis or postoperative recurrence. Small cancers with a high GGO ratio might be candidates for limited resection and a large multicenter study is necessary to confirm this postulate.
Limited resection has mostly been performed on patients with poor pulmonary reserve. Intentional limited surgery has not been common, particularly because lobectomy has been considered to be the standard treatment, which was confirmed by a randomized trial of the Lung Cancer Study Group [21]. However some successful results regarding limited surgery for T1 N0 tumors were published by Yamato who proposed limited resection for BAC by employing intraoperative pathological examination to confirm the absence of nodal metastasis [27]. They planned to convert limited resection to lobectomy if some invasive signs were recognized by frozen section. Tsubota performed extended segmentectomy for 55 patients with peripheral cancers measuring less than 2 cm in diameter and only 1 patient locally recurred in whom N2 disease was not indicated during operation [28]. Nakata performed thoracoscopic wedge resection for 33 pure GGO patients with tumors measuring less than 1 cm and no recurrence or metastasis was indicated during the follow-up period [12]. However well-differentiated adenocarcinomas or GGO-dominant tumors are considered to be indolent and slow-growing, therefore a long-term observation period is necessary to evaluate whether limited surgery could be an alternative to lobectomy.
In this study the ratio of GGO and consolidation on chest CT allows for the evaluation of the aggressive nature of small adenocarcinomas. However further investigation is required in this area, especially to characterize GGO on HRCT. Also genomic or proteomic studies are necessary to provide the clues to discriminate tumors with an indolent nature from those with an aggressive nature. Comprehensive research including pathology and molecular analysis will alter the conventional method of management regarding tiny cancers, which will be of great importance in daily practice.
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Acknowledgments
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The authors are indebted to Professor James Patrick Barron and Assistant Professor Raoul Breugelmans of the International Medical Communications Center at Tokyo Medical University (Tokyo, Japan) for their review of this manuscript.
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Abstract
Introduction
