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Right arrow Lung - cancer

Ann Thorac Surg 2003;75:1601-1605
© 2003 The Society of Thoracic Surgeons

Original article: general thoracic

Prospective study of thoracoscopic limited resection for ground-glass opacity selected by computed tomography

Masao Nakata, MDa*, Shigeki Sawada, MDa, Hideyuki Saeki, MDa, Shigemitsu Takashima, MDa, Hiroshi Mogami, MDb, Norihiro Teramoto, MDc, Kenji Eguchi, MDd

a Divisions of Surgery, Matsuyama, Japan
b Matsuyama, Japan
c Radiology, and Pathology, National Shikoku Cancer Center, Matsuyama, Japan
d Division of Pulmonary Medicine, Tokai University School of Medicine, Kanagawa, Japan

Accepted for publication November 11, 2002.

* Address reprint requests to Dr Nakata, Department of Surgery, National Shikoku Cancer Center, Horinouchi 13, Matsuyama, Ehime, 790-0007, Japan
e-mail: mnakata{at}shikoku-cc.go.jp


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
BACKGROUND: With recent advances in low-dose helical computed tomography (CT), detection of ground-glass opacity (GGO) has increased. The aim of this study was to correlate high-resolution CT (HRCT) findings with pathologic features and to evaluate the efficacy of thoracoscopic limited resection for focal GGO, which were selected based on HRCT findings.

METHODS: Focal GGO lesions were classified into two subtypes based on HRCT findings: pure type and mixed type. Ninety-six patients with persistent GGO 2 cm or less in diameter underwent pulmonary resection from January 1997 to December 2001. Among these, thoracoscopic wedge resection was performed prospectively between June 2000 and December 2001 in 33 patients with pure GGO lesions that were 1 cm or less.

RESULTS: Thoracoscopic wedge resection was completed with complete safety. The histologic diagnoses of these 33 lesions were adenocarcinoma in 1, bronchioloalveolar carcinoma (BAC) in 23, and atypical adenomatous hyperplasia (AAH) in 9. No patients have had any evidence of tumor recurrence to date. Of the total 96 GGO lesions, 93.0% (53/57) of pure GGO 1 cm or less were BAC or AAH, whereas 38.5% (15/39) of pure GGO larger than 1 cm or mixed GGO were adenocarcinoma.

CONCLUSIONS: Pure GGO 1 cm or less was characteristic of noninvasive lesions. Thoracoscopic limited resection for small GGO lesions selected by HRCT was valid.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
With recent advances in low-dose helical computed tomographic (CT) scans for lung cancer screening, there has been a noted increase in the detection of ground-glass opacity (GGO) in the peripheral lung [1–5]. When focal GGO is persistent after an observation period of several months, early adenocarcinoma or bronchioloalveolar carcinoma (BAC) is highly suspected [6, 7]. In the revised World Health Organization (WHO) histologic classification [8], BAC is classified as noninvasive carcinoma. Although the standard surgical procedure for lung cancer remains lobectomy with systemic lymph node dissection, limited resection could be justified when the entire tumor is noninvasive. However, these pathologic findings are of little use to select the candidate for limited resection because noninvasiveness can only be confirmed by postoperative microscopic examination. For the same reason noninvasiveness cannot be confirmed on preoperative small biopsy specimens, as described in WHO classification [8]. Therefore, the candidate for limited resection must be selected based on the CT findings. To date we have resected 96 patients with persistent focal GGO 2 cm or less in size. For 28 patients from January 1997 to May 2000, lobectomy with mediastinal node dissection was performed as a standard surgical procedure. On the basis of retrospective evaluation of radiologic and histologic findings of these 28 lesions, we made criteria for limited surgery and subsequently started a prospective study. Of 68 patients with focal GGO 2 cm or less from June 2000 to December 2001, thoracoscopic wedge resection was performed prospectively in 33 patients. The aim of this study was to evaluate the validity and oncologic efficacy of thoracoscopic limited resection for the focal GGO selected by high-resolution CT (HRCT) findings.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
Radiologic and pathologic classification
GGO was defined as a tumor with more than 50% consisting of hazy increased lung attenuation without obscuration of underlying vascular markings. Based on the HRCT findings, we classified GGOs into two subgroups: pure GGO, which consisted of only homogeneous translucent density (Fig 1), and mixed GGO, which consisted of heterogeneous attenuation with a solid component (Fig 2). Histologic diagnosis was made according to the revised WHO classification. BAC was defined as an adenocarcinoma with a bronchioloalveolar growth pattern and no evidence of invasive components. When an invasive component was identified, the tumor was classified as adenocarcinoma.



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  		Fig 1. Pure ground-glass opacity (GGO). A high-resolution computer tomographic scan revealed a homogeneous focal translucent GGO 9 mm in size. Histologic diagnosis was bronchioloalveolar carcinoma.

 


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  		Fig 2. Mixed ground-glass opacity. A high-resolution computed tomographic scan revealed a heterogeneous attenuation with solid components. Histologic diagnosis was well-differentiated adenocarcinoma 16 mm in size.

 
Preliminary retrospective study
From January 1997 to May 2000, 28 patients with persistent focal GGO 2 cm or less in diameter underwent pulmonary resection. The patients consisted of 9 male and 19 female, with a mean age of 58.0 years (range, 27 to 81 years old). These lesions were resected because they were not diminished after several months of observation (mean 3.7 months, 1 to 24 months). Surgical procedures were lobectomy with systematic lymph node dissection in 17 patients, segmentectomy with hilar node dissection in 2 patients, and wedge resection in 9 patients. The reasons for undergoing limited resection were intraoperative microscopic diagnosis of atypical adenomatous hyperplasia (AAH) in 6 patients, the presence of simultaneous multiple lung cancer in 1 patient, prior pulmonary resection due to lung cancer in 2 patients, and poor pulmonary reserves in 2 patients. Histologic diagnoses of 28 lesions were well-differentiated adenocarcinoma with mixed bronchioloalveolar pattern in 6 patients, BAC in 16 patients, and AAH in 6 patients. Radiologic characteristics and size distribution of GGOs are illustrated in Figure 3. There were 20 pure GGOs and 8 mixed GGOs. As depicted in Figure 3, all of the mixed GGOs were carcinoma. Sixteen lesions of pure GGO 1 cm or less were BAC or AAH except for one adenocarcinoma. Seventeen (5 adenocarcinoma and 12 BAC) of 22 carcinoma patients underwent lobectomy with systematic lymph node dissection, and no lymph node involvement was identified. The median follow-up period of 22 carcinoma patients was 44.8 months (range, 29 to 68 months). There has been no tumor recurrence or disease-related death. Based upon these findings, we concluded that pure GGO 1 cm or less could be a candidate for thoracoscopic limited resection and started a prospective study to justify these criteria since June 2000.



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  		Fig 3. Radiologic characteristics and size distribution of 28 ground-glass opacity (GGO) lesions. All of mixed GGOs were malignant. Sixteen lesions of pure GGO 1 cm or less were bronchioloalveolar carcinoma (BAC) or atypical adenomatous hyperplasia (AAH) except for one adenocarcinoma (AD). (S.D. = standard deviation.)

 
Patients
From June 2000 to December 2001, 72 patients were identified to have persistent focal GGO 2 cm or less after follow-up of several months (mean 4.2 months, 1 to 68 months). Except four patients who refused surgical intervention, 68 patients underwent pulmonary resection. The patients consisted of 21 male and 47 female, with a mean age of 61.6 years old (range 35 to 81 years old). On HRCT image, these lesions were categorized as 50 pure GGOs and 18 mixed GGOs. Preoperative diagnostic procedures including transbronchial biopsy and CT-guided percutaneous fine-needle biopsy were not performed in any patient. Forty-one of 68 patients were diagnosed as pure GGO 1 cm or less and 33 of these 41 patients underwent thoracoscopic wedge resection. Of the remaining 8 patients, 3 patients underwent segmental resection and 5 patients underwent lobectomy. The reasons for undergoing lobectomy were multiple lung nodules in the same lobe in 3 patients and requests from 2 patients. Twenty-seven GGO lesions not meeting the criteria for limited resection were resected by lobectomy with systematic lymph node dissection in 15, segmentectomy in 3, and wedge resection in 9. The reasons for undergoing wedge resection in 9 patients were the presence of simultaneous multiple lung cancers in 5 patients and several medical reasons in the other 4 patients.

Surgical technique of thoracoscopic limited resection
Thoracoscopic wedge resection was performed under one-lung ventilation using a double-lumen tube. When a lesion was not adjacent to the visceral pleura, CT-guided marking with hook-wire was performed immediately before operation. After insertion of three thoracoports, pulmonary resection was made using an endostapler with a surgical margin of at least 10 mm in the collapsed lung. When a surgical margin was thought to be sufficient macroscopically, the specimen was not submitted to intraoperative microscopic examination. No systematic lymph node dissection or sampling was performed. Definitive pathologic diagnosis was made with routine hematoxylin-eosin staining, because confirmation of noninvasiveness within entire lesion was difficult by intraoperative pathologic examination.

Follow-Up
Patients were followed at the outpatient clinic by chest Roentgenogram every 6 months and annual CT scans.

Data were analyzed using the unpaired Student’s t-test. Differences with a p value less than 0.05 were considered to be statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
In all the 33 patients who were intended for limited surgery, thoracoscopic wedge resection was completed without additional minithoracotomy. Preoperative CT-guided marking was efficient to localize the target lesion. There were no complications in preoperative marking except 2 patients with minor pneumothorax, which did not need any treatment. Surgical specimens were not submitted to intraoperative microscopic examination in any case. The histologic diagnoses of 33 lesions were well-differentiated adenocarcinoma in 1, BAC in 23, and AAH in 9. Pathologically negative surgical margins were obtained for all the specimens. There were no postoperative complications or operation-related death. The diagnoses of total 41 lesions of pure GGO 1 cm or less were adenocarcinoma in 3 patients, BAC in 28 patients, and AAH in 10 patients. There was no pleural invasion or lymphatic infiltration in any of the lesions.

The histologic diagnoses of 27 lesions not meeting the criteria for limited resection (9 lesions of pure GGO larger than 1 cm and 18 mixed GGO lesions) were well-differentiated adenocarcinoma in 8, BAC in 18, and AAH in 1. Five of 8 patients with adenocarcinoma had pleural invasion, and 1 lesion had lymphatic infiltration although lymph node metastasis was absent.

The median follow-up period of 33 patients undergoing thoracoscopic wedge resection was 18.0 months (range, 8 to 27 months). There has been no evidence of tumor recurrence or postoperative death in any of these patients to date. Also, 27 patients not meeting the criteria for limited resection are alive with no evidence of disease.

The patient characteristics of the total 96 GGOs are illustrated in Table 1. The majority of patients with focal GGO were female (68.8%) and nonsmoker (79.2%). The histologic diagnoses are illustrated in Table 2. Of 57 patients with pure GGOs 1 cm or less, 53 lesions (93.0%) were AAH or BAC, whereas 15 lesions (38.5%) were adenocarcinoma of the 39 of pure GGO larger than 1 cm or mixed GGO.


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  		Table 1. Patient Characteristics of the 96 Patients With Focal GGO

 

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  		Table 2. Histologic Diagnoses of the 96 GGO Lesions

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
Since the introduction of low-dose helical CT into the lung cancer screening, the detection of small lung cancer has been rapidly increasing [1–5]. Lung cancer detected by CT screening is mostly peripheral adenocarcinoma. Well-differentiated adenocarcinoma in early stage is often detected with hazy increased lung attenuation on HRCT, which is described as GGO. Several studies have already reported that persistent GGO suggests early adenocarcinoma or BAC [6, 7]. Our current study also demonstrated that persistent focal GGO after observation of several months was a finding of early adenocarcinoma or its precursor. When small GGO is detected at initial CT scan, we usually reevaluate it with HRCT at intervals of several months. Because an inflammatory lesion may resolve during these periods, it would be a helpful process in order to diagnose a small GGO lesion. However, when GGO was persistent after observation, all the cases in our series were neo-plastic lesions in spite of not performing preoperative biopsy. Lung biopsy or surgical intervention should be considered for persistent GGO lesions.

Lobectomy with systematic lymph node dissection remains the standard surgical procedure even for lung cancer small in size, because it has been reported that 10% to 20% of lung cancers 2 cm or less in size have lymph node metastasis [9]. The Lung Cancer Study Group [10] reported a higher incidence of locoregional recurrence after the limited resection for T1N0 lung cancer compared with lobectomy. However, with an increasing incidence of peripheral small lung cancer detected as GGO, whether lobectomy is necessary for tiny lung cancers has become another concern. In the revised WHO histologic classification [8], BAC is defined as a noninvasive carcinoma. If the entire tumor has no invasive component, limited resection could be the treatment of choice. However, because noninvasiveness can only be identified by postoperative microscopic study, the candidate for limited resection must be selected by preoperative HRCT imaging. In order to correlate the CT image with histologic findings, we continued performing lobectomy with mediastinal dissection for GGO lesions 2 cm or less until May 2000. In our retrospective study of initial 28 patients, we concluded that pure GGO 1 cm or less was a finding strongly suggesting noninvasive lesion, whereas mixed GGO suggested adenocarcinoma. Previously, we reported that solid component within GGO consisted of fibrosis or structural collapse of alveoli, which is often seen in adenocarcinoma [6]. Other reports have also suggested the diagnostic and prognostic value of central fibrosis in peripheral adenocarcinoma [11–13]. Based upon these results, we started a prospective study to evaluate the validity of thoracoscopic wedge resection for pure GGO 1 cm or less.

Thoracoscopic surgery is recognized as a minimal invasive procedure for pulmonary resection [14, 15]. A possible pitfall of thoracoscopic wedge pulmonary resection would be an insufficient surgical margin because of the difficulty in localizing the lesion. To prevent this surgical failure, preoperative CT-guided marking was a safe and useful method. In our series, all the lesions could be resected without additional thoracotomy, and negative surgical margins were obtained microscopically. The histologic diagnoses of 33 patients who underwent thoracoscopic wedge resection were noninvasive lesion except for one adenocarcinoma, which did not have vessel or lymphatic infiltration. In spite of short follow-up, tumor recurrence was not detected to date. These results indicated thoracoscopic wedge resection for small pure GGO lesions selected on HRCT findings was a feasible and valid alternative to standard lobectomy.

On the other hand, 27 lesions that did not meet our criteria for limited resection were diagnosed as 19 noninvasive lesions and 8 adenocarcinoma, of which 5 had pleural invasion or lymphatic infiltration. Of 39 lesions of pure GGO larger than 1 cm or mixed GGO in the total 96 lesions, 15 lesions (38.5%) were adenocarcinoma. These results also suggested the validity of our patient selection criteria. Although there was not any lymph node involvement in our current study, mediastinal lymph node metastasis were reported even in nonsmall cell lung cancer 1 cm or less in diameter [9, 16]. Therefore, lobectomy with mediastinal dissection is still the treatment of choice for mixed GGO and pure GGO larger than 1 cm. Whether segmentectomy could be an alternative to lobectomy deserves future evaluation [17].

Our current study has provided some issues on the approach to treatment of small GGO lesions. First, it provides an insight for improving treatment of multiple lung tumors. GGO is often found to be multicentric [18, 19]. It is crucial for treatment of multiple lung cancer to select the surgical procedure that is curative as well as conservative of pulmonary function. Our selection criteria for limited resection could be beneficial, considering the treatment of simultaneous or potential metachronous multiple lung cancers. Second, our current study provides another important issue of the treatment strategy for noninvasive lesions. When a noninvasive lesion can be identified on HRCT, careful observation without surgical intervention would be one of the choices. Our study demonstrated that persistent pure GGO 1 cm or less was a finding of noninvasive lesion, which could be the candidate for course observation. However, the natural history of GGO remains unknown, although sequential development of AAH to invasive adenocarcinoma is suspected [20, 21]. Aoki and coworkers [22] reported that 83% of BAC detected as focal GGO on HRCT had a tumor doubling time of more than 1 year. Hasegawa and colleagues [23] also reported that mean volume doubling time of GGO detected on mass CT screening was 813 days. In order to evaluate the necessity of surgical intervention for small GGO lesions as well as to develop an efficient follow-up system, understanding the biology of these lesions would be inevitable.

In conclusion, pure GGO 1 cm or less was a finding of noninvasive lesion. Thoracoscopic wedge resection for small pure GGO selected on HRCT findings was a valid procedure. The numbers of small GGO detected by low-dose helical CT screening will likely continue to increase. Further studies in large numbers should be encouraged in order to develop the adequate therapeutic strategy for these lesions.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

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  4. Sone S., Li F., Yang Z.-G., et al. Results of three-year mass screening programe for lung cancer using mobile low-dose spiral computed tomography scanner. Br J Cancer 2001;84:25-32.[Medline]
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  7. Kuriyama K., Seto M., Kasugai T., et al. Ground-glass opacity on thin-section CT. Value in differentiating subtypes of adenocarcinoma of the lung. AJR 1999;173:465-469.[Abstract/Free Full Text]
  8. Travis WD, Colby TV, Corrin B, et al. Histological typing of lung and pleural tumours. In: WHO international histological classification of tumors. 3rd edition. Geneva: Springer; 1999:25–47
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N. Ikeda, J. Maeda, K. Yashima, M. Tsuboi, H. Kato, S. Akada, and S. Okada
A clinicopathological study of resected adenocarcinoma 2 cm or less in diameter
Ann. Thorac. Surg., September 1, 2004; 78(3): 1011 - 1016.
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 Ann. Thorac. Surg.Home page
S. Yamada and T. Kohno
Video-assisted thoracic surgery for pure ground-glass opacities 2 cm or less in diameter
Ann. Thorac. Surg., June 1, 2004; 77(6): 1911 - 1915.
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 ChestHome page
M. Endo, Y. Kotani, M. Satouchi, Y. Takada, T. Sakamoto, N. Tsubota, and H. Furukawa
CT Fluoroscopy-Guided Bronchoscopic Dye Marking for Resection of Small Peripheral Pulmonary Nodules
Chest, May 1, 2004; 125(5): 1747 - 1752.
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 Eur. J. Cardiothorac. Surg.Home page
E. Johnson
Bronchioloalveolar carcinoma: myths and realities in the surgical management
Eur. J. Cardiothorac. Surg., January 1, 2004; 25(1): 147 - 147.
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 Eur. J. Cardiothorac. Surg.Home page
F. Barlesi, C. Doddoli, J.-P. Kleisbauer, and P. Thomas
Reply to Johnson
Eur. J. Cardiothorac. Surg., January 1, 2004; 25(1): 148 - 148.
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