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(Chest. 2000;117:779-785.)
© 2000 American College of Chest Physicians

Synchronous Roentgenographically Occult Lung Carcinoma in Patients With Resectable Primary Lung Cancer*

Philippe Pierard, MD; Philippe Vermylen, MD; Thierry Bosschaerts, MD; Candice Roufosse, MD; Thierry Berghmans, MD; Jean-Paul Sculier, MD, PhD and Vincent Ninane, MD, PhD

* From the Chest Service, CHU of Charleroi, Charleroi (Dr. Pierard); Departments of Internal Medicine (Drs. Berghmans and Sculier) and Pathology (Dr. Roufosse), Institut Bordet; and Chest Service (Drs. Vermylen and Ninane) and Thoracic Surgery Service (Dr. Bosschaerts), Saint-Pierre Hospital, Brussels, Belgium.

Correspondence to: V. Ninane, MD, Chest Service, Saint-Pierre Hospital, Rue Haute, 322, 1000 Brussels, Belgium


   Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective: To assess the prevalence of synchronous roentgenographically occult lung carcinoma (ROLC) in patients with resectable roentgenographically visible lung cancer (RVLC).

Methods: Patients undergoing surgery for RVLC in the same University Hospital were prospectively evaluated before surgery by fluorescence bronchoscopy under local anesthesia to detect synchronous ROLC. All abnormal areas, with the exception of the RVLC, had biopsies made.

Results: From June 1996 to January 1999, 43 patients (male/female ratio: 1.7/1.0) were evaluated before lobectomy (n = 34) or pneumonectomy (n = 10) for 44 primary RVLC. There were 10 T1N0, 19 T2N0, 1 T1N1, 9 T2N1, 1 T3N0, 3 T1N2, and 1 T3N1 lesions. The histologic type was mainly squamous carcinoma (n = 21) and adenocarcinoma (n = 14). All but two patients were smokers or ex-smokers (mean ± SD, 48 ± 28 pack-years). A total of 177 endobronchial biopsies were performed (4.1 ± 2.5); 8 were too small to be informative, 43 showed non-preneoplastic alterations, and 50 were normal. There were 7 basal cell hyperplasias, 56 metaplasias, 9 dysplasias, and 4 carcinomas in situ (CIS). All the dysplasias and CIS lesions were observed in eight subjects. The synchronous CIS were treated by surgery (n = 1) or localized therapeutic modalities (n = 3).

Conclusions: The high prevalence of synchronous early lung cancers (9.3%) as well as metaplasia and dysplasia in this series of patients with resectable RVLC suggests that fluorescence bronchoscopy may be a useful adjunct in the preoperative evaluation of lung cancer.

Key Words: fluorescence bronchoscopy • lung cancer • roentgenographically occult lung cancer


   Introduction
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 Introduction
Materials and Methods
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Roentgenographically occult lung cancers (ROLC) are early stage carcinomas, either carcinoma in situ (CIS) or T1 stage (TIS).1 Until recently, they were most often detected by positive sputum cytology, but the increasing use of conventional white-light bronchoscopy, as well as the development of new endoscopic methods including fluorescence bronchoscopy,2 has become an additional and growing means of identifying cases. ROLC are most often squamous cell carcinomas and are also characterized by a high incidence of synchronous lesions, ranging from 7 to 14%,3 4 5 6 7 and metachronous lesions, approximately 5% per year.5 6

The rate of second lung cancer after successful treatment of a first roentgenographically visible primary lung cancer (RVLC) is also elevated, with rates from 1 to 5% per year.8 9 10 11 12 13 The prevalence of ROLC synchronous to these RVLC, however, remains largely unknown. We postulated that this rate might not be negligible and that, after successful treatment of a first cancer, part of the second tumors might result from progressive evolution of synchronous, undetected preneoplastic lesions or ROLC. With this hypothesis in mind, we have assessed, with fluorescence bronchoscopy, patients with primary lung cancers before surgical resection. The technique of fluorescence bronchoscopy was chosen because it allows the detection of preneoplastic lesions and early lung cancers (CIS or microinvasive carcinoma) with a higher sensitivity than conventional white-light bronchoscopy.2


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
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Patients with suspected lung cancer on plain radiographs and CT scans underwent complete diagnostic and staging procedures, including conventional white-light bronchoscopy and lung function tests. At the end of the diagnostic and staging procedures, the surgeon had to consider the lesions as resectable.

Fluorescence bronchoscopy (Olympus BF20D; Light Induced Fluorescence Endoscopy; Xillix LIFE Imaging system; Vancouver, Canada) was then performed while the patient was comfortably seated in a 30° recumbent position in a high-backed armchair. Oral consent was required before the procedure. Oxygen (2 L/min) was administered with nasal prongs throughout the procedure, and transcutaneous hemoglobin saturation and cardiac rhythm (Ohmeda Biox 3740; Louisville, CO) were continuously monitored. In the absence of contraindication, 0.5 mg of atropine sulfate was also administered IV.14 No sedative agent was administered, and the whole procedure was accomplished on an outpatient basis.15

Atomized lidocaine (10% solution) was administered to achieve upper airways anesthesia, and local anesthesia of the tracheobronchial tree was obtained by instillation of 2% lidocaine solution throughout the larynx with a curved needle. Supplemental doses of lidocaine solution were administered as required through the operating channel of the bronchoscope. The bronchoscope was always introduced through the mouth to avoid the risk of nasal bleeding that can interfere with fluorescence examination. The whole procedure always began with careful examination of the trachea and the bronchial tree up to the subsegmental divisions under white-light and was followed by fluorescence examination and then by biopsies of all the areas suspected of being preneoplastic lesions or CIS.2 15 Examination was performed by operators experienced with this technique who, most often, had not been involved in the first diagnostic or staging conventional white-light bronchoscopy. Changes that were considered abnormal during white-light bronchoscopy included areas presenting an increase in redness, or a thickening or irregularity of the mucosa as well as nodular or polypoid lesions. During fluorescence examination, all the areas with heterogeneous aspects or homogenous defects were considered as suspect. All biopsies were fixed in formalin, embedded in paraffin, and classified into the following categories: normal, reserve cell hyperplasia, metaplasia, dysplasia, or CIS.16 17 We also encountered pathologic lesions such as inflammation or scarring processes that were classified as non-preneoplastic changes.

Statistical assessments were made using {chi}2 tests for homogeneity (categorical variables). Data are presented as mean ± SD. The criterion for statistical significance was taken as p < 0.05


   Results
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 Abstract
 Introduction
 Materials and Methods
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From June 1996 to January 1999, 52 patients underwent resection for primary lung cancer at Saint-Pierre University Hospital. Nine of these patients were not evaluated preoperatively by fluorescence bronchoscopy because of patient’s refusal (n = 1), presumed benign (vascular) disease (n = 1), or provisional unavailability of the technique (n = 7). In one of these nine patients presenting with left upper lobe squamous cell carcinoma, however, a left pneumonectomy was required, and microinvasive carcinoma was found during surgery at the resection margin. An additional resection toward the main carina was performed, but the margin was still characterized by persistent microscopic CIS. It must be stressed that, in this particular case, no abnormality had been observed at the level of the left mainstem bronchus during the initial diagnostic conventional white-light bronchoscopy. In the 43 patients assessed with fluorescence bronchoscopy, 44 lesions had been detected on plain radiographs and CT images. A first diagnostic or staging conventional white-light bronchoscopy had been performed in 42 patients and had revealed no additional endobronchial abnormalities suggestive of synchronous cancer. Table 1 illustrates the characteristics of the 43 patients (mean age, 63 ± 10 years; 27 men and 16 women) included in the present study. All but two of them were smokers or ex-smokers (mean smoking exposure, 48 ± 28 pack-years). Lobectomy was performed in 34 cases and pneumonectomy in 10 cases. Pathologic staging revealed 10 T1N0, 19 T2N0, 1 T1N1, 9 T2N1, 1 T3N0, 3 T1N2, and 1 T3N1 lesions. The histologic type was mainly squamous cell carcinoma (21 cases) and adenocarcinoma (14 cases).


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  		Table 1.. Characteristics of Patients*

 
All 43 patients were able to complete the entire fluorescence examination procedure, including white-light bronchoscopy, followed by fluorescence examination and biopsies. Figure 1 is an example of white-light and fluorescence image of a CIS that failed to be detected during the initial diagnostic or staging white-light bronchoscopy. A total number of 177 biopsies were performed (4.1 ± 2.5), and the results of histologic examination are given in Figure 2 . Eight samples were too small to be informative. The morphologic assessment of the 169 assessable samples included 43 non-preneoplastic abnormalities and 50 normal biopsies. There were 7 basal cell hyperplasias, 56 metaplasias, 9 dysplasias, and CIS (Fig 2) . All the dysplasias and CIS lesions were observed in eight subjects of whom five were active smokers and three were former smokers (Fig 3 ). No significant relationship was found between smoking habits (no smoking, previous, or current smoking) and the prevalence of significant preneoplastic lesions (dysplasia) or CIS.



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  		Figure 1.. Right upper lobe under white-light (Top) and fluorescence (Bottom) bronchoscopy in patient 43 evaluated just before surgical resection of a left upper lobe carcinoma. Irregularities of the anterior wall are present under white-light examination, and a large brown defect (normal tissue is represented by green color) corresponding to a CIS was noted during the following fluorescence examination. These abnormalities were missed during the initial diagnostic and staging conventional white-light bronchoscopy. The CIS was treated by PDT 1 month after left upper lobectomy.

 


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  		Figure 2.. Number of biopsies according to histologic results in the patient population. Other = pathologic lesions such as inflammation or scarring processes; RCH = reserve cell hyperplasia; MET = metaplasia; DYS = dysplasia.

 


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  		Figure 3.. Distribution of abnormal epithelia in the patient population. As can be seen, CIS were found in four patients, and all the DYS and CIS lesions (DYS or worse) were observed in eight subjects. Abbreviations are defined as in Figure 2 .

 
Table 2 shows the localization, greatest dimension, and treatment modality of the ROLC together with the localization and histology of resected RVLC in the four patients with synchronous CIS. In fact, with the exception of patient 16, in whom lobectomy allowed resection of both the proximal CIS and the peripheral RVLC, localized therapeutic modalities that conserve lung function were preferred and applied a few weeks after surgery in the three other patients, including photodynamic therapy (PDT) (n = 2) or endobronchial brachytherapy (n = 1). The first patient with synchronous ROLC was treated 1 year later for mediastinal recurrence by external radiotherapy. At that time, complete remission of the CIS was confirmed by biopsies. He died suddenly soon after. Two other patients (patients 16 and 32) are in complete remission of their ROLC and RVLC confirmed by radiographs and fluorescence bronchoscopy with endobronchial biopsies, whereas the last patient (patient 43) still requires evaluation.


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  		Table 2.. Clinicopathologic Features of ROLC*

 

   Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The present study shows that patients with resectable RVLC evaluated with fluorescence bronchoscopy have a high prevalence of synchronous ROLC (9.3%) and preneoplastic lesions. In each case, ROLC had to be considered as a primary tumor in nature because they were always CIS. Fluorescence bronchoscopy, a new diagnostic tool, was chosen inasmuch as it allows the detection of ROLC as well as preneoplastic lesions with a high sensitivity.2 15 18 Indeed, in our own experience,15 the relative sensitivity of white-light bronchoscopy followed by fluorescence bronchoscopy vs white-light bronchoscopy alone was 3.75 for intraepithelial neoplastic lesions. The positive predictive value of white-light bronchoscopy followed by fluorescence bronchoscopy in the detection of preneoplastic lesions has, however, been shown to be low,15 18 and this explains the large number of additional biopsies required in the present study (Fig 2) . However, the high negative predictive value of white-light bronchoscopy, followed by fluorescence bronchoscopy, suggests that this technique will miss a low number of significant lesions.15 18 The present study also did not include lung cancer patients with advanced, unresectable disease because we believe that fluorescence examination would be of little or no benefit and would only cause additional trouble for these patients.

One may argue that the population studied was small. In fact, it is as large as the series that have allowed the establishment of the frequency of multicentric lesions of ROLC. Multiple synchronous ROLC cancers were indeed found in four patients (7%), as reported by Cortese and colleagues,4 and in seven patients (15%), as reported by Martini and Melamed.3 On this basis, we can also conclude that the prevalence of synchronous ROLC in our series of patients with resectable RVLC seems to be as high as the previously reported prevalence of synchronous multiple lung cancers of ROLC. Lam and colleagues,2 using fluorescence bronchoscopy in a group of 53 patients with known or suspected lung cancer, also found synchronous CIS in 15% of them, but the way this cohort was selected and the characteristics of the suspected or known lung cancers, including their clinical stage, were not defined. We do not think that the use of fluorescence bronchoscopy, a new diagnostic tool, is the sole explanation for the high prevalence of synchronous ROLC in the present study. In fact, it is likely that synchronous ROLC are most often underdiagnosed in cases of RVLC during white-light examination, at least in part, because the bronchoscopist’s attention is focused on histologic confirmation of the diagnosis and endobronchial delimitation of neoplastic extension. An additional reason may be related to the fact that not all bronchoscopists are trained in recognizing early lung cancers. Some observations from the present study indeed support this hypothesis. During the initial diagnostic or staging conventional white-light bronchoscopy, no additional endobronchial abnormalities suggestive of synchronous cancer had been reported by the bronchoscopists. The fluorescence procedure also included white-light examination immediately before fluorescence examination. Attention of our particularly trained bronchoscopists was now turned toward identification of early lesions synchronous to the RVLC, and three of the four ROLC already showed subtle abnormalities that were magnified by fluorescence examination (Fig 1) . The condition seems quite different in cases of ROLC suspected on the basis of positive sputum cytology. Bronchoscopic inspection for localization of ROLC is then probably performed with particular attention because it is also known that associated changes of the mucosa are most often subtle. Indeed, in the initial studies on ROLC,5 the first white-light bronchoscopy failed to reveal any abnormality suggestive of cancer in approximately 70% of patients with positive sputum cytology. Despite some progress in the detection of these early lung cancers in relationship with a better knowledge of their appearance, a recent study reported that more than one white-light bronchoscopy was still required to localize ROLC detected by positive sputum cytology in as many as 39% of the cases.19

The present findings also have potential clinical implications. After successful resection of a first RVLC, the rate of second tumor has been shown to be elevated, with rates ranging from 1 to 5% per year.8 9 10 11 12 13 Unfortunately, despite closer follow-up in these patients, a curative resection of second lung cancers can only be performed in 50% of the cases, mainly because of poor pulmonary function or dissemination at the time of diagnosis.20 There is thus a need for close and prolonged follow-up in these patients that would allow detection of second cancers at earlier stages, when local treatments may be applied with curative intent. The present findings suggest that detection of second cancers should be initiated at the time the first cancer is diagnosed. Indeed, in eight of the patients (19%), we found significant intraepithelial lesions (dysplasia and CIS) that might progress, in a proportion and with a rapidity that remain largely unknown, to invasive carcinoma.21 Some answers may in fact arise from a better knowledge of the molecular biology of pulmonary preneoplastic lesions. This is well illustrated by recent studies on the expression of Bcl-2, whose gene is involved in the regulation of apoptosis, showing that Bcl-2-positive ROLC had a better prognosis than Bcl-2-negative ROLC.22 Even if some data suggest that CIS may regress to normal mucosa,23 24 a therapeutic option was chosen in each of our cases. On the other hand, close follow-up with repeat fluorescence bronchoscopies and biopsies were performed in cases of dysplasia. Whether this strategy will effectively reduce the incidence of metachronous lung cancers (by curative treatment of synchronous ROLC) and increase the relative number of early stage metachronous lung cancers (by follow-up and detection of progression of preneoplastic lesions with fluorescence bronchoscopy) will, however, require further studies.

With the exception of one patient in whom localization of both ROLC and peripheral RVLC in the same lobe allowed resection of both cancers by lobectomy, localized therapeutic modalities were preferred. In two patients, additional pulmonary resection was, in fact, contraindicated because of poor lung function. Endobronchial brachytherapy was preferred to PDT in one of these two patients because of the important endobronchial longitudinal extent of the CIS that has been shown to be associated with decreased success of PDT.25 In the third patient, PDT was chosen as an alternative to surgery for at least three reasons. First, surgical resection of both lesions would have implied a right pneumonectomy, a procedure that is associated with a higher mortality rate (approximately 10%) than right upper lobectomy.26 Second, a lung function sparing procedure might be preferred in cases of ROLC because of the high incidence of metachronous lesions,5 6 and third, PDT might be a good alternative to surgery in ROLC,27 in particular in cases of CIS.

In conclusion, the present study has shown that, in patients with resectable RVLC, the prevalence of synchronous preneoplastic lesions and early lung cancers is high and that fluorescence bronchoscopy may be a useful adjunct in the clinical staging of these patients. Further studies are required to assess the effect of early detection and treatment of synchronous ROLC on the incidence of metachronous cancers in these patients and on survival.


   Footnotes
 
Abbreviations: CIS = carcinoma in situ; PDT = photodynamic therapy; ROLC = roentgenographically occult lung cancer; RVLC = roentgenographically visible lung cancer;

Supported by Grants 9.4587.95, 7.4523.96, and 7.4512.98 from the Fonds National de la Recherche Scientifique (FNRS)-Télévie and by the Vésale Foundation, Belgium.

Received for publication April 13, 1999. Accepted for publication October 1, 1999.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Speiser, BL (1997) Strategies for treatment of occult carcinomas of the endobronchus. Chest 111,1158-1161[Free Full Text]
  2. Lam, S, MacAulay, C, Hung, J, et al (1993) Detection of dysplasia and carcinoma in situ with a lung imaging fluorescence endoscope device. J Thorac Cardiovasc Surg 105,1035-1040[Abstract]
  3. Martini, N, Melamed, MR (1980) Occult carcinomas of the lung. Ann Thorac Surg 30,215-223[Abstract]
  4. Cortese, DA, Pairolero, PC, Bergstalh, EJ, et al (1983) Roentgenographically occult lung cancer: a ten-year experience. J Thorac Cardiovasc Surg 86,373-380[Abstract]
  5. Woolner, LB, Fontana, RS, Cortese, DA, et al (1984) Roentgenographically occult lung cancer: pathologic findings and frequency of multicentricity during a 10-year period. Mayo Clin Proc 59,453-466[ISI][Medline]
  6. Saito, Y, Nagamoto, M, Ota, S, et al (1992) Results of surgical treatment for roentgenographically occult bronchogenic squamous cell carcinoma. J Thorac Cardiovasc Surg 104,401-407[Abstract]
  7. Usuda, K, Saito, Y, Nagamoto, N, et al (1993) Relation between bronchoscopic findings and tumor size of roentgenographically occult bronchogenic squamous cell carcinoma. J Thorac Cardiovasc Surg 106,1098-1103[Abstract]
  8. . and the Lung Cancer Study GroupThomas, P, Rubinstein, L (1990) Cancer recurrence after resection: T1N0 non-small cell lung cancer. Ann Thorac Surg 49,242-247[Abstract]
  9. Pastorino, U, Infante, M, Maioli, M, et al (1993) Adjuvant treatment of stage I lung cancer with high-dose vitamin A. J Clin Oncol 11,1216-1222[Abstract/Free Full Text]
  10. Thomas, PA, Rubinstein, L (1993) Malignant disease appearing late after operation for T1N0 non-small-cell lung cancer. J Thorac Cardiovasc Surg 106,1053-1058[Abstract]
  11. Antakli, T, Schaefer, RF, Rutherford, JE, et al (1995) Second primary lung cancer. Ann Thorac Surg 59,863-867[Abstract/Free Full Text]
  12. Ginsberg, RJ, Rubinstein, LV (1995) Randomized trial of lobectomy versus limited resection for T1N0 non-small cell lung cancer. Ann Thorac Surg 60,615-623[Abstract/Free Full Text]
  13. Martini, N, Bains, MS, Burt, ME, et al (1995) Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J Thorac Cardiovasc Surg 109,120-129[Abstract/Free Full Text]
  14. Reed, AP (1992) Preparation of the patient for awake flexible fiberoptic bronchoscopy. Chest 101,244-253[Free Full Text]
  15. Vermylen, P, Pierard, P, Roufosse, C, et al (1999) Detection of bronchial preneoplastic lesions and early lung cancer with fluorescence bronchoscopy: a study about its ambulatory feasibility under local anesthesia. Lung Cancer 25,161-168[CrossRef][ISI][Medline]
  16. Woolner, LB (1993) Lung. Henson, DE Albores-Saavedra, J eds. Pathology of incipient neoplasia 2nd ed. ,16-42 Saunders Philadelphia, PA.
  17. Colby TV, Koss MN, Travis WD. In situ and early invasive (occult) squamous cell carcinoma. In: Tumors of the lower respiratory tract: atlas of tumor pathology. 3rd series, fascicle 13. Washington, DC: US Armed Forces Institute of Pathology, 1995:145–155
  18. Lam, S, Kennedy, T, Unger, M, et al (1998) Localization of bronchial intraepithelial neoplastic lesions by fluorescence bronchoscopy. Chest 113,696-702[Abstract/Free Full Text]
  19. Bechtel, JJ, Kelley, WR, Petty, TL, et al (1994) Outcome of 51 patients with roentgenographically occult lung cancer detected by sputum cytologic testing: a community hospital program. Arch Intern Med 154,975-980[Abstract]
  20. Johnson, BE (1998) Second lung cancers in patients after treatment for an initial lung cancer. J Natl Cancer Inst 90,1335-1345[Abstract/Free Full Text]
  21. Saccomanno, G, Archer, VE, Auerbach, O, et al (1974) Development of carcinoma of the lung as reflected in exfoliated cells. Cancer 33,256-270[CrossRef][ISI][Medline]
  22. Chen, Y, Sato, M, Fujimura, S, et al (1999) Expression of Bcl-2, Bax, and p53 proteins in carcinogenesis of squamous cell lung cancer. Anticancer Res 19,1351-1356[ISI][Medline]
  23. Auer, G, Ono, J, Nasiell, M, et al (1982) Reversibility of bronchial cell atypia. Cancer Res 42,4241-4247[Abstract/Free Full Text]
  24. Band, PR, Feldstein, M, Saccomanno, G (1986) Reversibility of bronchial marked atypia: implication for chemoprevention. Cancer Detect Prev 9,157-160[ISI][Medline]
  25. Furuse, K, Fukuoda, M, Kato, H, et al (1993) A prospective phase II study of photodynamic therapy with Photofrin II for centrally located early-stage lung cancer. J Clin Oncol 11,1852-1857[Abstract/Free Full Text]
  26. Kopec, SE, Irwin, RS, Umali-Torres, CB, et al (1998) The postpneumonectomy state. Chest 114,1158-1184[Free Full Text]
  27. Edell, ES, Cortese, DA (1992) Photodynamic therapy in the management of early superficial squamous cell carcinoma as an alternative to surgical resection. Chest 102,1319-1322[Abstract/Free Full Text]



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