Chest ACCP Career Connection
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (18)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Liu, Y.-Y.
Right arrow Articles by Perng, R.-P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Liu, Y.-Y.
Right arrow Articles by Perng, R.-P.
(Chest. 2000;118:940-947.)
© 2000 American College of Chest Physicians

Prognosis and Recurrent Patterns in Bronchioloalveolar Carcinoma*

Yung-Yang Liu, MD; Yuh-Min Chen, MD, PhD, FCCP; Min-Hsiung Huang, MD, FCCP and Reury-Perng Perng, MD, PhD, FCCP

* From the Chest Department (Drs. Liu, Chen, and Perng), Thoracic Surgery Section (Dr. Huang), Veterans General Hospital-Taipei, and National Yang-Ming University, School of Medicine, Taipei, Taiwan, ROC.

Correspondence to: Yuh-Min Chen, MD, PhD, FCCP, Chest Department, Veterans General Hospital-Taipei, 201, Sec. 2, Shih-Pai Rd, Taipei, Taiwan, ROC; e-mail: ymchen{at}vghtpe.gov.tw


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: Bronchioloalveolar carcinoma (BAC) is an uncommon pulmonary neoplasm with various radiologic and clinical presentations. In this article, we analyze the initial radiologic findings, TNM stagings, surgical types, and radiologic features of recurrence, and correlate them with patient survival.

Design: A retrospective review of 93 patients who underwent resection for BAC from February 1989 to May 1999.

Patients: There were a total of 153 patients with BAC diagnosed during this period. Among them, 60 patients (39.2%) had diffuse disease and received medical therapy only, and the remaining 93 patients (60.8%), who had localized disease, underwent surgical resection. Patients who received surgical resection were enrolled in this study.

Measurements: Data regarding demographics, presentation symptoms, initial radiologic features, surgical type, tumor staging, recurrence status, radiologic patterns of recurrence, and survival were obtained from all patients.

Results: Female patients were significantly younger than male patients. Patients who were female, nonsmoking, undergoing curative surgery, lobectomy, or bilobectomy, and with early tumor staging and no nodal involvement had a better prognosis. Patients with a right lung tumor had a longer survival than those with a left lung tumor, with borderline significance. Among those who suffered from recurrent diseases, a second resection yielded a better survival. Multivariate analysis showed curative surgery, initial surgical type, recurrence status, radiologic patterns of recurrence, and duration from surgical resection to recurrence all had a significant impact on survival.

Conclusions: Those patients with localized, early-stage BAC who underwent curative surgery had a better survival. Patients with localized recurrence after the initial surgery warranted a second resection. Those with a diffuse radiologic pattern of recurrence and/or early recurrence had a worse prognosis.

Key Words: bronchioloalveolar carcinoma • recurrence • survival • thoracic surgery


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Bronchioloalveolar carcinoma (BAC) is an uncommon primary malignant pulmonary neoplasm, and it accounts for 2 to 14% of all pulmonary malignancies.1 2 It was first described by Malassez3 in 1876, as a bilateral, multinodular form of malignant lung tumor. In 1903, Musser4 discovered another form: a diffuse, infiltrative type of BAC involving a single lobe or the entire lung simulating pneumonia. In 1953, Storey et al5 recognized that the most frequent form was a solitary peripheral pulmonary nodule, and BAC was then disclosed as having three different major radiologic patterns.

According to World Health Organization categorization, BAC is a subtype of adenocarcinoma. The current definition of BAC is similar to the entity described by Liebow6 in 1960 and includes the following: malignant neoplasms of the lung that have no evidence of extrathoracic primary adenocarcinoma, an absence of a central bronchogenic source, a peripheral parenchymal location, no distortion of the pulmonary interstitium, and neoplastic cells growing along the alveolar septa. The origin of the malignant cells is still controversial, and both unicentric and the multicentric hypotheses have been postulated. However, one article7 favored a monoclonal origin for multifocal disease. It is generally accepted that BAC represents two distinct clinical entities of identical histologic appearance.8 9 The solitary or focal form has a better prognosis following curative resection and less progress toward diffuse disease; the diffuse form (multinodules, diffuse, or infiltrating) tends to be relentlessly progressive with a worse prognosis regardless of intervention.8 9 10 11 12 However, the previous literature mentions little about whether or not recurrent characteristics, such as early or late recurrence, recurrent radiologic patterns, and salvage surgery, could affect the patient’s survival.

In this study, we reviewed Chinese BAC patients who had received surgical resection, to investigate the natural course of BAC following surgery and to analyze the prognostic factors of the disease. The importance of salvage surgery is also discussed.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
We retrospectively reviewed and analyzed the chart records and computer files of patients with a pathologic diagnosis of BAC following surgery at Veterans General Hospital-Taipei from February 1989 to May 1999. Veterans General Hospital-Taipei is a general teaching hospital with > 2,500 beds. During the study period, BAC was diagnosed in 153 patients and 93 patients received surgical resection as the initial treatment modality. The preoperative workup included chest radiograph, fiberoptic bronchoscopy, pulmonary function test, chest CT scan, bone scan, and brain CT scan. All patients met the histopathologic criteria for a diagnosis of BAC, ie, an absence of an identifiable primary malignancy elsewhere, an absence of endobronchial carcinoma, a pattern of malignant cells growing along the alveolar walls, and preservation of the general interstitial framework of the lung.13 Papillary tumors with well-developed fibrovascular cores were classified as papillary adenocarcinoma and excluded from the present study.

Each patient’s clinical characteristics, including age, gender, smoking history, initial presenting symptoms, and the duration of symptoms before surgery, were recorded. All preoperative chest radiographs were reviewed to determine the presenting radiologic features of BAC. The radiologic features of BAC were classified as either nodular or infiltrating forms. The lesion was classified as an infiltrating form if it was a poorly delineated opacity without defined borders. A well-circumscribed lesion completely surrounded by pulmonary parenchyma was classified as a solitary pulmonary nodule. The type of surgery, surgical staging, recurrence status, location and radiologic pattern of recurrence, and the length of time from initial surgery to recurrence were all recorded. Each patient’s disease was staged according to the TNM staging system.14 Curative surgery was defined as a total removal of visible and/or palpable lesion(s) based on the surgeon’s judgment, and the cut-end was free from tumor according to the pathologic report. Patients were followed until their death or last follow-up. Survival was defined as the time between date of surgery and date of death.

For the statistical study, the Kaplan-Meier method with a log-rank test was used for survival analysis, the Cox-regression method was used for multivariate survival analysis, and the Mann-Whitney test was used as a nonparametric test. SPSS statistical software (SPSS; Chicago, IL) was used for these analyses.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
One hundred fifty-three cases of BAC were diagnosed in our hospital from February 1989 to May 1999. Among them, 60 patients (39.2%) had diffuse disease and received medical treatment only. The remaining 93 patients (60.8%), who had localized disease, underwent surgical resection initially. Of these 93 patients studied, 54 were men (58%) and 39 were women (42%), with a mean age of 66.9 years (range, 42 to 89 years). Female patients (63.2 ± 9.6 years) were significantly younger than male patients (69.6 ± 7.7 years; p = 0.002). Forty-one patients (44%) had a history of cigarette smoking. Forty patients (43%) were asymptomatic at the time of diagnosis. Cough was the most common presenting symptom (28 patients; 30.1%), followed by hemoptysis (12 patients; 12.9%), chest pain (6 patients; 6.5%), body weight loss (2 patients; 2.2%), and dyspnea (2 patients; 2.2%). Another three patients (3.2%) presented with delayed resolution of pneumonia. The mean duration of symptoms was 11.8 weeks (range, 0 to 107 weeks).

The pattern and frequency of the initial chest radiologic presentations of these 93 surgically resected BAC patients are listed in Table 1 . A solitary peripheral nodule was the most frequent finding, occurring in 79 cases (84.9%), followed by an infiltrating or pneumonic mass in 11 cases (11.8%), multinodular lesions of the same side of the lung in 2 cases, and a mass with cavity in 1 case. The most frequent location of the tumor was the right upper lobe (37.6%), followed by the left upper lobe (22.6%), the right lower lobe and the left lower lobe (both 15.1%), and the right middle lobe (7.5%).


View this table:
[in this window]
[in a new window]

  		Table 1.. Initial Chest Radiologic Patterns and Locations of 93 Surgically Resected BACs*

 
Sixty-four patients (68.8%) underwent a complete lobectomy, 9 patients underwent a bilobectomy for tumor involvement of the adjacent lobe, 6 patients underwent a pneumonectomy because of extensive disease or metastatic nodules found during the surgery, 7 patients underwent a lobectomy plus wedge resection due to a tumor involving the adjacent lobe or a suspected metastatic lesion found on the neighboring lobe during the surgery, and the remaining 7 patients underwent a wedge resection of the solitary peripheral nodule only. The results of pathologic staging after surgery are shown in Table 2 . Thirty-nine patients (41.9%) suffered from disease recurrence during the follow-up period. All the recurrent cases had the same histologic finding of primary tumor. There was no other histologic type of lung cancer found during the follow-up period. The radiologic presentations of the 39 recurrent diseases were multiple nodules in 13 patients, a solitary nodule or mass in 8 patients, an infiltrating or pneumonic mass in 4 patients, a miliary lesion in 4 patients, mixed alveolar and nodular opacity in 4 patients, lymphangitic spreading in 4 patients, pleural effusion in 1 patient, and rib destruction in 1 patient (Table 3 ). Among these patients, the radiologic patterns of the recurrent diseases of 33 primary solitary nodular diseases were as follows: multiple nodules in 11 patients, solitary nodule in 8 patients, miliary in 4 patients, lymphangitic spreading in 4 patients, infiltrating or pneumonic mass in 3 patients, mixed alveolar and nodular opacity in 1 patient, bone destruction in 1 patient, and pleural effusion in 1 patient. The radiologic patterns of the recurrent diseases of four primary infiltrating or pneumonic masses were the same as the primary disease in one patient, and mixed alveolar and nodular opacity in three patients. The recurrent pattern was same as primary disease in the patient who suffered from primary multiple nodular disease. The pattern changed to multiple nodules without cavity in the patient whose primary disease was a mass with cavity formation. Among them, eight patients underwent a secondary surgical resection for localized recurrence.


View this table:
[in this window]
[in a new window]

  		Table 2.. Pathologic Staging of 93 Surgically Resected BACs*

 

View this table:
[in this window]
[in a new window]

  		Table 3.. Chest Radiologic Patterns of 39 Recurrent BACs After Surgery

 
The median survival of all 93 patients with resections was 295 weeks. The overall survival curve is shown in Figure 1 . Survival analysis showed a significantly longer survival among female patients (n = 39) than male patients (n = 54; median survival, 295 weeks vs 259 weeks; p = 0.026). There was also a significant difference in the survival of patients with (n = 41) or without (n = 52) a history of smoking (median survival, 259 weeks vs > 300 weeks; p = 0.043). Different presenting symptoms did not affect patient survival significantly (p = 0.745), nor did symptomatic (median survival, 338 weeks) or asymptomatic (median survival, 295 weeks; p = 0.557) diagnoses. Initial chest radiologic patterns did not correlate with patient survival (p = 0.263). The median survival of those with a solitary nodular lesion was 295 weeks, and the median survival of those with infiltrating and multiple nodular lesions was 359 weeks. Patients with an initial tumor location at the right lung had a longer survival than those with a left lung tumor, with borderline significance (median survival, 359 weeks vs 188 weeks; p = 0.057; Fig 2 ). Patients who underwent curative surgery had longer survival than those who received noncurative surgery (median survival, 314 weeks vs 124 weeks; p = 0.004; Fig 3 ). Patients who underwent a lobectomy or bilobectomy had significantly longer survival than those with other surgical procedures (p = 0.017; Fig 4 ). Both nodal involvement and staging status had a significant impact on survival (p = 0.0019 and p = 0.002, respectively). Five-year survival for the 61 stage I patients was 68%; and 5-year survival for the 9 stage II patients was 26.7%. The 4-year survival of the 13 stage III patients was 29.5%, and the 4-year survival of the 8 stage IV patients was 0. Patients who suffered from recurrent disease had significantly poorer survival than those without recurrence (p = 0.0001; Fig 5 ). Among those patients who suffered from recurrent disease, those who received a second resection survived longer than those without a second surgical procedure (median, 314 weeks vs 133 weeks; p = 0.044; Fig 6 , top, A). The median time from first operation to recurrence (disease-free survival) was longer in those who received a second operation than in those without (87 weeks vs 55 weeks; p = 0.104).



View larger version (9K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1.. Survival curve of 93 resected BACs using the Kaplan-Meier method. The median survival time was 295 weeks.

 


View larger version (11K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2.. Kaplan-Meier survival curve of 93 resected BACs by location (log-rank test; p = 0.057): right lung BAC (n = 57; median survival, 359 weeks), and left lung BAC (n = 36; median survival, 188 weeks).

 


View larger version (9K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3.. Kaplan-Meier survival curve of 93 resected BACs by curative surgery status (log-rank test; p = 0.004): curative resection (n = 83; median survival, 314 weeks), and no curative resection (n = 10; median survival, 124 weeks).

 


View larger version (14K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 4.. Kaplan-Meier survival curve of 93 resected BACs by surgical type (log-rank test; p = 0.017): lobectomy (n = 64; median survival, 314 weeks), bilobectomy (n = 9; median survival, 338 weeks), pneumonectomy (n = 6; median survival, 119 weeks), and wedge and lobectomy (n = 7; median survival, 124 weeks). The median follow-up time of the seven patients who received wedge resection was only 62 weeks.

 


View larger version (11K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 5.. Kaplan-Meier survival curve of 93 resected BACs by recurrence status (log-rank test; p = 0.0001): recurrence (n = 39; median survival, 175 weeks). The median survival of the 54 nonrecurrence patients is still not available; 70.6% are still alive at 300 weeks.

 


View larger version (16K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 6.. Kaplan-Meier survival curve of 39 recurrent BACs by salvage surgery status. Top, A: survival time calculated from the date of first operation to their death or last follow-up. The median survival time of the 8 salvage surgery patients was 314 weeks, and 133 weeks in the 31 patients without a salvage operation (p = 0.044). Bottom, B: survival time calculated from date of recurrence to the death or last follow-up. The median survival time of the 8 salvage surgery patients was 105 weeks, and 46 weeks for the 31 patients without a salvage operation (p = 0.082).

 
In the multivariate analysis using the Cox-regression method, we analyzed age, sex, smoking history, presenting symptoms, duration of presenting symptoms, initial radiologic patterns, initial tumor location, curative resection status, surgical type, T status, N status, M status, stage, recurrence status, recurrence radiologic pattern, whether or not there was a second surgery, and the length of time from surgery to recurrence. We found that curative resection (p = 0.0001; R = -0.228), surgical type (p = 0.007; R = 0.148), metastatic status (p = 0.009; R=-0.143), recurrence status (p = 0.007; R = 0.148), radiologic pattern (p = 0.008; R = 0.145) of recurrence, and length of time from surgery to recurrence (p = 0.0002; R = -0.218) significantly determined the prognosis of our patients.

We then performed another survival analysis, with survival time calculated from the finding of recurrence to the patient’s death or last follow-up, for the 39 patients who suffered from recurrence. The median survival time for the 8 patients who received a second resection was 105 weeks, and 46 weeks for the 31 patients without a second operation (p = 0.082; Fig 6 , bottom, B). Chest radiologic findings of recurrent disease had a significant impact on patient survival (p < 0.0001). Median survival was longest in the 4 patients with combined alveolar and nodular patterns (188 weeks), followed by solitary nodule or mass (8 patients; 105 weeks), miliary patterns (4 patients; 54 weeks), infiltrating or pneumonic patterns (4 patients; 41 weeks), multinodular patterns (13 patients; 32 weeks), and lymphangitic spreading (4 patients; 9 weeks). The data are shown in Table 3 . Multivariate analysis using sex, smoking history, time from first operation to recurrence, recurrent radiologic patterns, and whether there was a second surgery or not were done. Only radiologic patterns of recurrence had a significant impact on survival (p = 0.031; R = 0.1317).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
BAC was formerly considered a mystery tumor because of its various radiologic, clinical, and cytopathologic manifestations. Barkley and Green15 have reported that BAC appears to be increasing in incidence, especially in young female patients. We found that our female BAC patients were significantly younger than the male BAC patients. We also found that female patients have a significantly longer survival than male patients.

Patients with a history of cigarette smoking have a decreased survival rate compared to nonsmokers. It is hard to explain why nonsmokers had a better survival rate than smokers. Smokers did not suffer from a higher incidence of recurrence (Pearson’s {chi}2 test; p = 0.558). On the contrary, nonsmokers had more advanced disease than smokers in the beginning (Pearson’s {chi}2 test; p = 0.031). The longer survival of nonsmokers might be related to better cardiovascular and pulmonary functions, as compared to smokers. However, sex and smoking status did not affect patient survival in the multivariate analysis.

Forty patients (43%) in our study were asymptomatic at the time of diagnosis. Their survival was not significantly different from those with symptoms. The median survival was shorter in asymptomatic patients, however, than in those with symptoms (295 weeks vs 338 weeks). Whether or not the presence or absence of symptoms is a prognostic factor is still a controversial issue.1 Cough, hemoptysis, and chest pain were the most common complaints in our study, and this finding is essentially the same as that of the study by Regnard et al.1 However, we had only three patients who initially presented with a delayed resolution of pneumonia. This percentage is much lower than that reported by Regnard et al,1 in that 13 of 70 patients with resections in their study presented with pneumonia. Of course, we had another eight patients whose initial radiologic pattern was infiltrating or pneumonic mass. If we consider these patients together with the three patients presenting with a delayed resolution of pneumonia, the incidence of pneumonia in the initial presentation was similar in both studies. It is acknowledged that the radiologic appearance of BAC includes focal nodular(s) or mass(es), and pneumonic and diffuse patterns; therefore, BAC should be considered in the differential diagnosis of solitary or multiple nodules and acute or chronic alveolar diseases.2

BACs can be classified into mucinous, nonmucinous, and mixed or indeterminate cell types. It has been found that a prognosis of nonmucinous BAC is better than that of mucinous BAC, probably because the mucinous type tends to spread aerogenously and forms infiltrating, multifocal, or satellite tumors.15 16 17 18 19 We did not analyze this factor because the present study is limited to patients with surgical resections (it would likely distort the study population to have a higher proportion of nonmucin secretion BAC as compared to all patient groups) and focused on the study of clinical and radiologic prognostic factors.

At the present time, we still cannot explain why the right lung BAC patients survived better than the left lung BAC patients. Right lung BAC did not have less recurrence than left side BAC ({chi}2 test; p = 0.412), or an earlier staging status than left side BAC ({chi}2 test; p = 0.283).

Curative resection and the type of initial resection affected the patient’s survival significantly, both in our univariate and multivariate analysis. In our study, patients who underwent a curative resection, or lobectomy or bilobectomy, had a better survival than patients with other surgical procedures. Greco et al20 found that patients treated with less than a lobectomy have higher recurrence rates and a worse prognosis, and Barsky et al21 reported that lung-sparing procedures (wedge or segmentectomy) give the disease the propensity to recur in a multifocal origin. It can be concluded from our and other studies1 12 that the complete surgical resection of localized BAC offers the best chance of long-term survival. In addition, salvage surgery in patients who suffer from localized tumor recurrence is also suggested, based on our data showing better survival among those who received a second resection after recurrence.

Staging status is an important prognostic factor in BAC patients receiving surgical treatment.1 12 Clayton22 found that patients with a tumor size < 3 cm had a better outcome than those with a tumor size > 3 cm. Sutton et al23 reported that relatively long-term survivors had no histologic evidence of hilar or mediastinal lymph nodal involvement, compared to the other surgical cases. Our study also demonstrated that staging is an important prognostic factor. However, when TNM was considered separately, only nodal status had a significant impact on survival in univariate analysis, and metastatic status in multivariate analysis.

For those who suffered from recurrence, the longer the disease-free survival, the longer the overall survival. Recurrent radiologic patterns did have an impact on survival. Salvage resection in appropriate cases prolonged the patient’s overall survival significantly and improved survival time after recurrence, with borderline significance. Four of the patients with recurrent disease presented with lymphangitic carcinomatosis. It has been reported that lymphangitic carcinomatosis can occur during late or terminal stage of disease course, especially in nonmucinous BAC, displaying an interstitial pattern in addition to other radiographic abnormalities.15 24 25 26

In conclusion, female BAC patients were younger and had a better prognosis than male patients. The patients with localized, early-stage BAC who underwent curative surgery had a better outcome. Patients with a shorter duration between the first surgery and recurrence had a poorer prognosis. And, those with a localized recurrence after the surgery warranted a second resection.


   Footnotes
 
Abbreviation: BAC = bronchioloalveolar carcinoma

Received for publication November 8, 1999. Accepted for publication May 11, 2000.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Regnard, JF, Santelmo, N, Romdhani, N, et al (1998) Bronchioloalveolar lung carcinoma: results of surgical treatment and prognostic factors. Chest 114,45-50[Abstract/Free Full Text]
  2. Bonomo, L, Storto, ML, Ciccotosto, C, et al (1998) Bronchioloalveolar carcinoma of the lung. Eur Radiol 8,996-1001[CrossRef][ISI][Medline]
  3. Malassez, L (1876) Examen histologique d’un cas de cancer encephaloide du poumon (epithelioma). Arch Physiol Norm Pathol 3,353-372
  4. Musser, JH (1903) Primary cancer of the lung. Univ Penn Bull 16,289-296
  5. Storey, CF, Kundtsor, KP, Lawrence, BJ (1953) Bronchiolar (alveolar. cell) carcinoma of the lung. J Thorac Cardiovasc Surg 26,331-406
  6. Liebow, AA (1960) Bronchioloalveolar carcinoma. Adv Intern Med 10,329-358[Medline]
  7. Holst, VA, Finkelstein, S, Yousem, SA (1998) Bronchioloalveolar adenocarcinoma of lung: monoclonal origin for multifocal disease. Am J Surg Pathol 22,1343-1350[CrossRef][ISI][Medline]
  8. Epstein, DM (1990) Bronchioloalveolar carcinoma. Semin Roentgenol 25,105-111[CrossRef][ISI][Medline]
  9. Miller, WT, Husted, J, Freiman, D, et al (1978) Bronchioloalveolar carcinoma: two clinical entities with one pathologic diagnosis. AJR Am J Roentgenol 130,905-912[Abstract]
  10. Dumont, P, Gasser, B, Rouge, C, et al (1998) Bronchioloalveolar carcinoma: histopathologic study of evolution in a series of 105 surgically-treated patients. Chest 113,391-395[Abstract/Free Full Text]
  11. Albertine, KH, Steiner, RM, Radack, DM, et al (1998) Analysis of cell type and radiographic presentation as predictors of the clinical course of patients with bronchioloalveolar cell carcinoma. Chest 113,997-1006[Abstract/Free Full Text]
  12. Hsu, CP, Chen, CY, Hsu, NY (1995) Bronchioloalveolar carcinoma. J Thorac Cardiovasc Surg 110,374-381[Abstract/Free Full Text]
  13. World Health Organization. The World Health Organization histological typing of lung tumors. 2nd ed. Am J Clin Pathol 1982; 77:123–136
  14. Mountain, CF (1986) A new international staging system for lung cancer. Chest 89(suppl),225S-233S[Free Full Text]
  15. Barkley, JE, Green, MR (1996) Bronchioloalveolar carcinoma. J Clin Oncol 14,2377-2386[Abstract]
  16. Manning, JT, Jr, Spjut, HJ, Tschen, JA (1984) Bronchioloalveolar carcinoma: the significance of two histologic types. Cancer 54,525-534[CrossRef][ISI][Medline]
  17. Lee, KS, Kim, Y, Han, J, et al (1997) Bronchioloalveolar carcinoma: clinical, histopathologic, and radiologic findings. Radiographics 17,1345-1357[Abstract]
  18. Okubo, K, Mark, EJ, Flieder, D, et al (1999) Bronchoalveolar carcinoma: clinical, radiologic, and pathologic factors and survival. J Thorac Cardiovasc Surg 118,702-709[Abstract/Free Full Text]
  19. Travis, WD, Colby, TV, Corrin, B, et al (1999) Histological typing of lung and pleural tumours World Health Organization. 3rd ed. Springer Berlin, Germany.
  20. Greco, RJ, Steiner, RM, Goldman, S, et al (1986) Bronchoalveolar cell carcinoma of the lung. Ann Thorac Surg 41,652-666[Abstract]
  21. Barsky, SH, Grossman, DA, Ho, J, et al (1994) The multifocality of bronchioloalveolar lung carcinoma: evidence and implications of a multiclonal origin. Mod Pathol 7,633-640[ISI][Medline]
  22. Clayton, F (1988) The spectrum and significance of bronchioloalveolar carcinoma. Pathol Annu 23,361-394
  23. Sutton, LN, Morrison, JF, Rees, MR (1989) Radiographic features and prognosis in bronchioloalveolar carcinoma: a local experience. Respir Med 83,471-477[ISI][Medline]
  24. Decker, HR (1955) Alveolar-cell carcinoma of the lung (pulmonary adenomatosis). J Thorac Surg 30,230-247
  25. Berkmen, YM (1969) The many facets of alveolar-cell carcinoma of the lung. Radiology 92,793-798[ISI][Medline]
  26. Schulze, ES, Mattia, AR, Chew, FS (1994) Bronchioloalveolar carcinoma [letter]. Am J Radiol 162,1294[Free Full Text]



This article has been cited by other articles:


Home page
 J. Thorac. Cardiovasc. Surg.Home page
D. J. Raz, A. Y. Odisho, B. L. Franc, and D. M. Jablons
Tumor fluoro-2-deoxy-D-glucose avidity on positron emission tomographic scan predicts mortality in patients with early-stage pure and mixed bronchioloalveolar carcinoma.
J. Thorac. Cardiovasc. Surg., November 1, 2006; 132(5): 1189 - 1195.
[Abstract] [Full Text] [PDF]

Home page
 Eur. J. Cardiothorac. Surg.Home page
F. Barlesi, C. Doddoli, C. Gimenez, B. Chetaille, R. Giudicelli, P. Fuentes, J.-P. Kleisbauer, and P. Thomas
Bronchioloalveolar carcinoma: myths and realities in the surgical management
Eur. J. Cardiothorac. Surg., July 1, 2003; 24(1): 159 - 164.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
M. I. Ebright, M. F. Zakowski, J. Martin, E. S. Venkatraman, V. A. Miller, M. S. Bains, R. J. Downey, R. J. Korst, M. G. Kris, and V. W. Rusch
Clinical pattern and pathologic stage but not histologic features predict outcome for bronchioloalveolar carcinoma
Ann. Thorac. Surg., November 1, 2002; 74(5): 1640 - 1647.
[Abstract] [Full Text] [PDF]

Home page
 RadiologyHome page
M. Tsubamoto, K. Kuriyama, S. Kido, J. Arisawa, N. Kohno, T. Johkoh, N. Tomiyama, O. Honda, and C. Kuroda
Detection of Lung Cancer on Chest Radiographs: Analysis on the Basis of Size and Extent of Ground-Glass Opacity at Thin-Section CT
Radiology, July 1, 2002; 224(1): 139 - 144.
[Abstract] [Full Text]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (18)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Liu, Y.-Y.
Right arrow Articles by Perng, R.-P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Liu, Y.-Y.
Right arrow Articles by Perng, R.-P.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS