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Ann Thorac Surg 2002;73:386-392
© 2002 The Society of Thoracic Surgeons

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Original article: general thoracic

Natural history of pure ground-glass opacity after long-term follow-up of more than 2 years

^a Departments of Thoracic Surgery, Diagnostic Radiology, Field Research and Internal Medicine, Osaka Medical Center for Cancer and Cardiovascular Diseases, Osaka, Japan

Accepted for publication October 16, 2001.

* Address correspondence to Dr Kodama, Department of Thoracic Surgery, Osaka Medical Center For Cancer and Cardiovascular Diseases, 1-3-3 Nakamichi, Higashinari-ku, Osaka 537-8511, Japan
e-mail: kdm{at}ma2.justnet.ne.jp

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Background. Pure ground-glass opacity (PGGO) is a new entity that has been clearly defined on high-resolution computed tomography (CT) during the last half decade. It is important to investigate the natural history of PGGO through long-term observation for the management of this new entity.

Methods. We investigated 19 patients with PGGO(s) defined on high-resolution computed tomography and retained as PGGO for more than 2 years. The PGGOs of 11 patients were detected at annual mass screening by low-radiation–dose CT (low-dose CT), 7 at follow-up CT after cancer resection, and 1 incidentally on CT. After long-term observation, 10 of 19 patients underwent operation and 9 are currently being followed-up with CT. Their growth characteristics and histologic findings are reported.

Results. The median follow-up period was 32 months, ranging from 24 to 124 months. The sizes of PGGOs at the time of discovery were 4 to 18 mm in largest diameter (average 8.6 mm). During follow-up, the size of PGGO showed no change in 8 patients, increased slightly (up to 5 mm) in 6 patients, and increased by more than 5 mm in 5 patients. Ten patients had limited resection (segmentectomy or wide wedge resection) with negative surgical margin by intraoperative lavage cytology of the resection margin of the lung. Of them, 5 patients had adenocarcinoma, 3 pulmonary lymphoproliferative disorder, and 1 each atypical adenomatous hyperplasia and focal fibrosis. There was no clear tendency between the degree of size change and histology. In all but 1 of 9 patients with follow-up only, the PGGOs showed either no change or only a slight increase within 5 mm in largest diameter.

Conclusions. These data suggest that some PGGOs will never progress to clinical disease and would be included in the category of overdiagnosis bias. However, a prior history of lung cancer should significantly raise the index of suspicion, as 4 of 5 proven cancer cases in this small series fell into that category. Because of the difficulties of preoperative and intraoperative histodiagnosis of PGGO, minimally invasive surgery may be appropriate from the viewpoints of both diagnosis and curability.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
In 1997, Collins and associates [1] alphabetically listed 19 lesions showing ground-glass opacity on computed tomography (CT), including acute chest syndrome, bronchiolitis obliterans organizing pneumonia, cytomegalovirus and other pneumonias, and cancer and lymphoproliferative disorders, among many others. However, most of these show a diffuse or mixed (not solitary or pure) appearance. Solitary pure ground-glass opacity (PGGO), or solitary pure ground-glass attenuation (PGGA), shadow is a new entity that has been defined by high-resolution CT (HRCT) during the last half decade. In particular, small PGGOs ( 10 mm in largest diameter) were never detected by conventional chest roentgenography or early-generation CT.

To date, 49 patients with PGGO have been surgically treated at our institution. Most of them were discovered at annual screening using low-radiation–dose computed tomography (low-dose CT) or conventional CT during postoperative follow-up of lung cancer. After surgery for PGGO, most of them were histologically noninvasive bronchioloalveolar carcinoma (BAC) [2, 3] or atypical adenomatous hyperplasia (AAH) [4]. The most recent World Health Organization histologic typing of lung and pleural tumors has classified BAC as a noninvasive subtype of adenocarcinoma of the lung [5]. The counterpart with an invasive component was classified as adenocarcinoma with mixed subtypes.

Recently, Breathnach and colleagues [6] reported the favorable 5-year survival rate in patients with stage I BAC compared with the same stage of adenocarcinoma (83% versus 63%, p = 0.04). We recently reported the results of semiquantitative analysis of the GGO area in the adenocarcinoma as a useful independent prognostic indicator for deciding the operative method [7]. However, because of the short history of this new entity (PGGO), its natural history is completely unknown. Diligent long-term follow-up will be the only means to elucidate the natural history of PGGO and to determine whether surgical intervention is acceptable or unnecessary, ie, contributing to overdiagnosis bias [8–11].

The purpose of this study was to elucidate the natural history of PGGO cases which were detectable only on CT scan and were observed for more than 2 years.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Between January 1996 and March 2001, a total of 49 patients with PGGO underwent operation at our institution. When we defined the follow-up period as the duration from the first detection of PGGO on CT to the operation, the preoperative median follow-up period for those 49 patients was 6 months. Of those patients, 38 underwent operation within 18 months and 1 additional patient within 19 months.

The remaining 10 patients with long-term preoperative follow-up of more than 2 years were enrolled in this study to clarify the natural history of PGGO. An additional 9 patients whose PGGO is now under follow-up without operation for more than two years were also added to the present study. The estimated doubling time of asymptomatic solitary pulmonary nodules is usually less than 2 years. Thus, we thought that a longer follow-up more than 2 years would be sufficient to elucidate the natural history of PGGO.

Of the 19 patients with PGGO, 10 were men and 9 were women. The average age at the time of discovery of PGGO was 62 years (range 35 to 76 years). The patients underwent periodical CT, including the HRCT, throughout their clinical course or at an annual mass screening. When the size and density were unchanged on CT after 3 months, the next CT was scheduled for 6 months later. If no change was detected on the reexamination, the next CT was scheduled for 1 year later.

Pure ground-glass attenuation is defined as a shadow completely occupied with a hazy increased attenuation of the lung, with preservation of the bronchial and vascular margins in the lesion on HRCT [1]. When the PGGO is too small to palpate or is located inside of the lung parenchyma without any change in visceral pleural surface, preoperative marking under CT using a 1-mL to 2-mL cocktail with indocyanine green (25 mg/3 mL) and iohexol (300 mg/mL) was done beneath the pleura just above the target lesion.

	Results

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
The demographic characteristics of the 19 patients are presented in Table 1. Pure ground-glass attenuation was discovered at an annual mass screening using low-dose CT in 11 cases, at postoperative follow-up CT examination for lung cancer in 6 cases (patients 1 to 4, 9, and 12) and for renal cell carcinoma in 1 case (patient 17), and at CT taken incidentally in 1 case. In Patients 1 to 4 and 12, the PGGO was found in the contralateral lung of the operated site and, with the exception of patient 4, was confirmed by retrospective review of preoperative CT. The smaller PGGO in patient 9 was also confirmed in the operative site by retrospective review of preoperative CT.

The sizes of PGGOs at the time of discovery were 4 to 18 mm in largest diameter (average 8.6 mm) in the 17 patients with solitary PGGO. The largest diameters in the 2 patients with multiple PGGOs (patients 4 and 11) were 15 mm and 10 mm, respectively. During follow-up, the size of PGGO increased by more than 5 mm in 5 patients (Fig 1A and B), increased slightly (up to 5 mm) in 6 patients, and showed no change in 8 patients. Percutaneous needle aspiration cytology or histology were appropriate only in 3 patients because of the small, fine biopsy target. At each periodic examination, the advantages and disadvantages of surgical treatment, were discussed, and informed consent based on the individual PGGO characteristics was obtained. As a result, 10 patients agreed to receive surgical intervention. The remaining 9 patients elected to continue further follow-up because of the following reasons: no change in size or the PGGOs were less than 10 mm in patients 13, 14, and 17 to 19; lesions involving all lobes in patient 11; advanced age in patient 15; severe ulcerative colitis in patient 16; and poor pulmonary function in patient 12.

View larger version (142K): [in this window] [in a new window]   Fig 1. Computed tomogram from 57-year-old man (patient 1) with long-term follow-up of pure ground-glass opacity (PGGO) for more than 10 years. Patient had undergone operation for adenocarcinoma originating in right upper lobe 10 years previously. (A) Small PGGO in left upper lobe (arrow) was pointed out as a function of the retrospective review of conventional CT taken at that operation. (B) On follow-up 124 months later, high-resolution computed tomography shows enlargement of PGGO from 8 mm (A) to 25 mm in diameter. (C) Most of the resected specimen reveals bronchioloalveolar carcinoma (hematoxylin and eosin, x2.5). (D) Focus of invasive adenocarcinoma can also be recognized. (Hematoxylin and eosin, x66.)

The pathologic specimens demonstrated adenocarcinoma with mixed subtypes in 1 patient (patient 1), BAC in 4 (patients 2 to 5), lymphoproliferative disorder in 3 (patients 7 to 9), and AAH and focal fibrosis in 1 patient each (patients 6 and 10, respectively). Of note, four of five carcinomatous lesions were discovered at follow-up CT in the patients with previously resected lung cancer; these were considered as multiple primary lung cancers. The postoperative median follow-up for the 10 patients was 15 months. At present, 9 patients are alive withoutrecurrence. Patient 4, who had two lesions of BAC, died of stomach cancer 2 years after the segmentectomy without lung cancer recurrence.

Patient 1 had initially undergone operation for adenocarcinoma, with a diameter of 23 mm invading visceral pleura of the right upper lobe 124 months previously. His CT films taken before the first operation (Fig 1A) were reviewed retrospectively, and proved that his PGGO in the left upper lobe had increased during the long-term follow-up of more than 10 years (Fig 1B). The reason for the long-term follow-up was refusal of the operation by the patient. Eventually we received informed consent to the operation and successfully removed the PGGO of 25 mm diameter by wide wedge resection. Despite the increase in size, his lesion maintained the PGGO appearance on HRCT (Fig 1B) until operation. However, an invasive component was histologically demonstrated and diagnosed as adenocarcinoma with mixed subtypes (Fig 1C and D). Although a recurrence was recently discovered in this patient’s right thorax, it is considered to be late recurrence of the first cancer on which the operation was conducted 124 months previously.

A pulmonary lymphoproliferative disorder was found in 3 patients (patients 7 to 9). The disorder was subclassified as postinflammatory change with lymphoid hyperplasia in patient 7, as lymphoid interstitial pneumonia (LIP) in patient 8 (Fig 2), and as low-grade marginal zone B-cell lymphoma of the mucosa-associated lymphoid tissue in patient 9. The disorders included irregularly shaped air spaces surrounded by enlarged bronchioloalveolar septa with strong lymphocyte infiltration.

View larger version (77K): [in this window] [in a new window]   Fig 2. Computed tomogram from 35-year-old man (patient 8) with lymphoid interstitial pneumonia. (A) After 24 months of follow-up, high-resolution computed tomography shows slight enlargement (from 11 mm to 14 mm) in diameter of pure ground-glass opacity in middle lobe (arrow). (B) Resected specimen showing irregularly shaped multiple air spaces. (Hematoxylin and eosin, x2.5.) (C) Higher-power microscopic finding reveals irregular alveolar wall thickening due to dense infiltrate of small lymphocytes. (Hematoxylin and eosin, x66.)

View larger version (131K): [in this window] [in a new window]   Fig 3. Computed tomogram from 65-year-old-woman (patient 11) with multiple pure ground-glass opacities (PGGOs). (A) Multiple small PGGOs were found in all lobes of lung. Computed tomographic slice reveals three PGGOs (arrows) in the right upper lobe. The lobe, including the maximal PGGO (10 mm in diameter), was removed. (B) Comprehensive histologic examination of resected specimens demonstrated existence of many smaller lesions revealing bronchioloalveolar carcinoma or atypical adenomatous hyperplasia. (Hematoxylin and eosin, x66.) During 37 months of postoperative follow-up, only a slight increase in size or density was recognized in some residual PGGOs scattered in all lobes.

	Comment

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Randomized controlled trials of lung cancer screening using chest radiography have consistently shown an excessive number of cancer cases as well as longer survival in screened groups, but no difference in mortality between screened and control populations [12].

Henschke and colleagues [8] reported that, compared with chest radiography, low-dose CT greatly increases the likelihood of detection of small noncalcified nodules and, thus, of lung cancer at an earlier and more curable stage. On low-dose CT, noncalcified nodules were detected three times as often as on chest radiography, malignant tumors four times as often, and stage I tumors six times as often. Moreover, the malignant tumors detected on low-dose CT were substantially smaller than those detected on chest radiography, even within stage I. When noncalcified nodules are discovered on low-dose CT, we usually conduct HRCT to estimate the quality of the nodules. As a result, PGGO came to be identified as one subgroup of such noncalcified nodules, and the incidence of discovery has dramatically increased in the last half decade. A focal area of ground-glass opacity found on HRCT could be considered as an early sign of BAC [2, 3]. However, the natural history of the lesion occupied completely by ground-glass opacity (ie, PGGO) has remained unknown. The present study was conducted to elucidate the natural history and the histologic characteristics of PGGOs observed for more than 2 years.

From our experience, if the PGGO is due to acute inflammation or bleeding, it usually disappears during the initial 3-month follow-up period. When the PGGO shows an increase in size or density at 3 to 6 months of follow-up, we usually recommend that the patient undergo diagnostic intervention or thoracotomy to completely remove the lesion, as a choice of management. Transthoracic biopsy guided by CT has offered an alternative to open surgical biopsy for preoperative diagnosis. Although rare, tumor dissemination after CT-guided biopsy is a potential risk [13]. Use of this diagnostic modality should be considered on an individual basis in light of the operative risk as well as the potential for curative resection [13]. On the other hand, when PGGO remained the same size and density for 3 months or more, periodic follow-up using CT should be an option, based on considerations of lesion size at discovery and patient factors such as age, cardiopulmonary function, or coexistence of other diseases. As 4 of 5 patients (patients 1 to 4) with proven cancers in this study had a prior history of lung cancer, postoperative PGGO in lung cancer patients should be closely monitored.

In 1997, we reported the feasibility of segmentectomy as an intentional limited resection for selected patients with small lung cancers [14]. Because patient enrollment was completed in September 1996, only one BAC with PGGO was included in that cohort for analysis. The incidence of the discovery of PGGOs has dramatically increased since 1996. Because of a lack of clinical data regarding this new entity, we are advancing a prospective study on the feasibility of limited resection such as wide wedge resection or segmentectomy in combination with preoperative CT marking and intraoperative lavage cytology of the resection margin [15]. Given the high success rate (only one error among 41 procedures to date), we believe that our marking method is a more reliable as well as a less expensive method for detecting nonvisible and nonpalpable intrapulmonary lesions. Of course, we always confirm the complete removal of the target lesions by postoperative follow-up CT. It is often difficult to perform intraoperative histodiagnosis by using frozen sections. The PGGO is too small and soft; thus it is extremely difficult to accurately choose a suitable site for freezing. We therefore believe that the lavage cytology is preferable here. If a positive finding is obtained on lavage cytology, we prefer standard lobectomy to limited resection. We believe that this treatment modality will decrease the risk of local recurrence at the resection margin of the lung.

Elective thoracotomy of smaller stage I lung cancers is less costly than treatment of later-stage lung cancers, most of which require a combination of radiotherapy and chemotherapy and may necessitate thoracotomy [8]. As a step toward the goal of therapy for patients with PGGO, it is important to elucidate the natural history of PGGO, especially to avoid overdiagnosis bias. Thus, management of PGGO (which never include early-stage aggressive cancers such as small cell carcinoma or undifferentiated carcinoma) should be different from management of small, peripheral, noncalcified solitary nodules showing soft-tissue density on CT.

In conclusion, when the size of PGGO remains stable or increases only slightly over the long term, a variety of histologic entities, from BAC to benign lesions such as lymphoproliferative disorder or focal fibrosis, should be considered. A prior history of lung cancer should significantly raise the index of suspicion, as four of five proven cancers in this small series fell into that category. However, because of the difficulties of preoperative or even intraoperative histodiagnosis of small PGGO, wide wedge resection or segmentectomy in combination with intraoperative lavage cytology of the resection margin of the lung should be recommended as a safe and minimally invasive method in the treatment of PGGO.

	Acknowledgments

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
This study was partially funded by a Grant-in-Aid for Cancer Research (13–9) from the Ministry of Health, Labour and Welfare, Japan.

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments 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): Ken Kodama Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kodama, K. Articles by Imamura, F. Search for Related Content PubMed PubMed Citation Articles by Kodama, K. Articles by Imamura, F. Related Collections Lung - cancer Related Article