Journal of Surgical Oncology 48:75-80 (1991)

Early Hilar Lung Cancer: Its Clinical Aspect YOH WATANABE, MD, JUNZO SHIMIZU, MD, MAKOTO ODA, MD, TAKASHI IWA, MU, TSUTOMU TAKASHIMA, MD, RYOlCHl KAMIMURA, MD, MASANOBU KITAGAWA, MD, AKITAKA NONOMURA, MD, SHINOBU NAKAMURA, MD, KAZUO TANIMOTO, MD, FUJITSUGU MATSUBARA, MD, SHIGERU IKEGAKI, MD, AND KATUJI YAMADA, MD From the Departments of Surgery (Y.W., I.S., M.O., 7.1.1, Radiology (T.T., R.K.), and Clinical Pathology (M.K., A.N., S.N., K.T., F.M.), Kanazawa University School of Medicine, Kanazawa; Department of Surgery, Wajima City Hospital (S.I.), Wajima; and Department of Radiology, Matto Municipal Hospital (K.Y.1, Matto, Ishikawa, lapan

Early hilar lung cancers are rare, but are curable if they are properly diagnosed and treated. In the past 14 years, we have treated 27 patients with early hilar cancers that fulfilled the criteria proposed by the Japanese Lung Cancer Society (JLCS). Eighteen patients presented with symptoms and 9 were detected by the mass screening examination of sputum cytology. All lesions in both groups were finally diagnosed by bronchoscopy. Twenty patients (74%) had positive sputum cytology, whereas only 7 (26%) had positive chest X-ray findings. All the patients underwent surgery, and bronchoplasty was the most frequent operative procedure. The 5-year survival rate was loo%, and the 10-year survival rate was 91.7%, as one patient died of a second primary lung cancer in the 6th postoperative year. In conclusion, the definition of early hilar lung cancer proposed by the JLCS is thought to be reasonable, and early hilar lung cancer is a curable disease, if it is properly diagnosed and treated. KEYWORDS:sputum cytology, mass screening examination, bronchoscopy, operation, limited bronchial resection

INTRODUCTION Early cancers in the hilar region are rare, but they are curable if they are properly diagnosed and treated. Most of the cancers in this region do not produce any abnormalities on chest X-ray films, but they often are associated with symptoms such as hemoptysis or dry cough. Furthermore, in contrast to peripheral cancers of the lung, hilar tumors can be definitively diagnosed by sputum cytology and bronchoscopy . An internationally accepted set of criteria for early hilar cancer has not been determined as yet, but the Japanese Lung Cancer Society (JLCS) has produced their own set of criteria. We experienced our first case of early hilar lung cancer which fulfilled the JLCS criteria in 1977. Since then, we have treated 27 patients with early hilar lung cancer. The patients in the earlier half of the present series were detected at the outpatient department after investigation of symptoms or by an abnormality on the chest film. A mass screening program for the early detection of lung cancer was started in 1984 in our 0 1991 Wiley-Liss, Inc.

prefecture, so that the latter half of the present series contained both symptomatic patients and asymptomatic patients detected by screening. This article discusses the clinical features, diagnostic methods, and results of surgical management. In addition, a rationality of the JLCS criteria in defining early hilar lung cancer is discussed.

MATERIALS AND METHODS In defining early hilar lung cancer, the criteria proposed by the JLCS were used. The JLCS define early hilar lung cancers as tumors that fulfill the following three histological criteria: 1) the lesion is localized proximal to the segmental bronchi; 2) the depth of tumor invasion is confined to within the bronchial wall; and 3 ) Accepted for publication February 15, 1991. Address reprint requests to Yoh Watanabe, MD, Department of Surgery, Kanazawa University School of Medicine, 13- 1 Takaramachi, Kanazawa 920, Japan.

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there are no lymph node metastases or distant metastases. From 1977-1990, we treated 27 patients with early hilar lung cancer, which corresponded to 2.7% of all lung cancer patients admitted and 3.5% of those undergoing resection. The 27 patients included both symptomatic patients who underwent bronchoscopic examination when they visited our outpatient department and asymptomatic patients who were detected by the prefectural mass screening program, mostly by positive sputum cytology. At our outpatient department, all the patients with respiratory complaints routinely underwent bronchoscopic examination. Bronchial washings and brushings as well as bronchial biopsy specimens were obtained for a definitive diagnosis. In the mass screening program of our prefecture, the high risk group for hilar lung cancer was defined as men more than 45 years of age, with a smoking index of over 500 (average number of cigarettes smoked per day X years of smoking history), or with a history of hemoptysis in the previous 6 months. For the high risk group, cytological examination of a 3-day sputum collection was performed in addition to routine examination of the chest X-ray film. All the patients were finally diagnosed by histological examination of bronchial biopsies taken using a bronchofiberscope. Preoperative bronchoscopic examination was crucially important in determining the extent of these lesions, because most of them could not be seen nor be palpated from outside the bronchus at operation. For the exact determination of the extent of the disease, several biopsy specimens or smears were taken from the mucosa adjacent to the cancer. The bronchoscopic findings of the lesion were classified into three types: 1) superficial type; 2) nodular type; and 3) polypoid type. All the 27 patients underwent surgical treatment. Sleeve lobectomy and standard lobectomy were the operative procedures used for most of the patients, but a few patients with very small localized lesions underwent limited bronchial resection [ 11. Microscopic examination of serial sections of the resected specimens was performed to determine the final diagnosis of early hilar lung cancer as well as the extent of each lesion. Another nine patients had lesions that were initially thought to be early hilar cancer, but were shown to have minute invasion outside the bronchial wall by microscopic examination of serial sections. We designated such lesions as “semiearly” cancer and we have excluded these nine patients from the present study. The 27 patients were divided into two groups: patients whose tumors produced symptoms (symptomatic group) and patients whose lesions were detected by mass screening (mass screening group). The clinical background factors, methods of detection, and clinical features were compared between these groups.

The survival rate of the patients was calculated by the Kaplan-Meier method.

RESULTS The 27 patients with early hilar lung cancer consisted of 26 males and 1 female. Eighteen were in the symptomatic group and the other 9 were in the mass screening group, There were 23 smokers and 4 nonsmokers, and the smoking index of the smokers ranged from 400-3,600 (average: 957). The chief complaints noted in the symptomatic group were hemoptysis in eight patients, cough in eight, and fever in two. The pathological features of the 27 tumors are shown in Table I. Twenty-six patients had squamous cell carcinoma and 1 had mucoepidermoid carcinoma. The lesions of 8 patients were carcinoma in situ and those of the other 19 patients were invasive carcinoma confined to within the bronchial wall. The smallest lesion in the present series was a polypoid lesion of 1 mm in diameter (carcinoma in situ), which was detected in a 61-year-old male who complained of massive hemoptysis 10 days before his admission (Fig. 1). Twenty patients had positive sputum cytology, whereas in 7 patients malignant cells were detected by cytological examination of the sputum. Seventeen cancers were on the right side and 12 were on the left side including two second primary lesions. Figure 2 is a diagram showing the locations of these 29 tumors. On the right side, 11 lesions were located in the upper lobe, 1 in the middle lobe, and 5 in the lower lobe bronchi. On the left side, 8 lesions were located in the upper lobe bronchi, 3 in the lower lobe bronchi, and 1 at the second carina. The left-sided group included two double primary early lung cancers, one synchronous, and one metachronous. One patient had a lesion in the right upper lobe bronchus combined with a tiny synchronous second primary lesion in the left upper lobe bronchus. The second patient had a lesion in the right upper lobe bronchus and a metachronous second primary lesion in the left upper lobe bronchus developed 5 years after the first operation. In Table 11, the clinical background features are compared between the symptomatic group (n = IS) and the mass screening group (n = 9). None of the patients in the mass screening group had any symptoms. Abnormal chest X-ray film findings were noted in 6 patients of the symptomatic group, and in only one of the mass screening group, so no abnormality was detected in 12 members of the symptomatic group and 8 of the mass screening group. Sputum cytology in 11 of 18 patients in the symptomatic group was positive, whereas all 9 patients in the mass screening group had positive sputum cytology. All the lesions in both groups were detected at bronchoscopy, and all were diagnosed histologically by preoperative bronchial biopsy. The bronchoscopic findings were 6

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TABLE I. Pathological Features of Early Hilar Lung Cancer

Histology Squamous cell carcinoma Mucoepidermoid carcinoma Extent of invasion Carcinoma in situ Invasion of bronchial wall Sputum cytology Positive Negative Location Right lung Left lung

26 1 8 19 20 7 17

12a

Two second primary cancers (one synchronous and one metachronous) are included.

a

Fig. 2. Diagram showing the locations of 29 early hilar lung cancers in 27 patients. Their locations on the right side were 11 lesions in the right upper lobe, 1 in the middle lobe, and 5 in the right lower lobe bronchi. On the left side, there were 8 lesions (including 1 second primary lesion) in the left upper lobe, 3 in the left lower lobe bronchi, and 1 at the second carina.

TABLE 11. Comparison of Clinical Features Between the Symptomatic and Asymptomatic Patients Symptomatic Mass screening group group In = 18) (n = 9)

Fig. 1. Microscopic findings of a polypoid carcinoma in situ about I mm in diameter which was detected in a 61-year-old male who complained of hemoptysis. The tumor occupied the orifice of right B6 and histology was squamous cell carcinoma.

superficial type, 10 nodular type, and 11 polypoid type (Fig. 3). The polypoid type in the mass examination was relatively small in number in comparison with that in the symptomatic group. Table 111 shows the treatment for each of the 29 lesions including the two double primary cancers. The most frequently performed procedure was a sleeve lobectomy and this was followed by standard lobectomy. Two patients with tiny lesions at the orifice of the segmental bronchus underwent sleeve segmentectomy . In addition, a lesion located at the bifurcation of the left upper and lower lobe bronchi was successfully treated by second carinal resection without lung resection. Postoperative pulmonary function tests (conventional pulmonary function test, ventilation scan, and perfusion scan) in these

Symptoms Positive Negative Chest X-ray film Positive Negative Sputum cytology Positive Negative Bronchoscopy Positive Superficial type (n = 6) Nodular type (n = 10) Polypoid type (n = 11) Negative

18 0

0 9

6 12

8

11 7

9 0

18 3

9 3

6

4

9

2

0

0

1

three patients clarified almost completely preserved lung function. There was no operative morbidity or mortality in the present series. One patient underwent bilateral sleeve

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Fig. 3. Bronchoscopic views of three types of the early hilar cancer. Left, superficial type. Middle, nodular type. Right, polypoid type. A, epithelial layer; B, subepithelial layer; C, muscular layer; D, submuscular layer; E, cartilage.

lobectomy for metachronous double primary cancers at an interval of 6 years [2]. These procedures were tolerated well and the patient has survived 12 years since the first operation and 6 years since the second. The patient with synchronous double primary cancer had the lesion in the right upper lobe bronchus resected by sleeve lobectomy and the lesion in the left upper lobe bronchus (a 2 mm carcinoma in situ) was cauterized by YAG laser by bronchoscopy. He is still alive and well 49 months after the treatment. Two patients developed metachronous second primary cancer of the lung. One patient died of a second primary cancer after surviving over 5 years from the time of operation. When the second lesion was detected, the disease was far advanced for the second surgical intervention. He underwent radiotherapy for the second lesion, but there was no apparent effect. He died of the second cancer at the 6th postoperative year after the first operation. The other was the patient mentioned above. Figure 4 shows the survival curves of the 27 patients

with early hilar lung cancer. The 5-year survival rate was 100% and the 10-year survival rate was 91.7%.

DISCUSSION Generally speaking, early cancer should be defined as a tumor that is compatible with long-term survival after the treatment. There is as yet no internationally approved definition of early lung cancer. However, there have been several reports concerning occult lung cancer, in which category occult adenocarcinoma of the peripheral bronchi, hilar squamous cell carcinoma with extrabronchial invasion, and even lesions having nodal or distant metastases were included [3-61. Accordingly, the 5-year survival rate was far less than 100%. The definition of early hilar lung cancer proposed by the JLCS appears to be a reasonable one, because no patient developed recurrent cancer or suffered cancer death during the first 5 years after treatment. Except for one rnucoepidermoid carcinoma, all the tumors in the present series were

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TABLE 111. Treatment of 29 Early Hilar Lung Cancers

Sleeve lobectomy Standard lobectomy Sleeve segmentectomy Second carinal resection Second sleeve lobectomy Laser surgery a

15 9 2

-

80

1 la lb

For a metachronous second primary cancer. For a tiny synchronous second primary cancer.

20

i h squamous cell carcinomas. There was only one female among the 27 patients with early hilar lung cancer. In the detection of these lesions, conventional chest X-ray studies, sputum cytology, and bronchofiberscopy were employed. Conventional chest X-ray films were positive in only 33% (6 of 18) of the symptomatic group and 11% (1 of 9) of the mass screening group, so chest X-ray was not a useful method for the detection of early hilar lesion. In contrast, sputum cytology was positive in 74% (20 of 27) of the symptomatic patients and in all the mass screening group. There is some controversy concerning the clinical value of mass screening programs for the early detection of lung cancer [7,8]. In our district, mass screening was started in 1984, and since then 19 patients with early hilar lung cancer have presented. Of these 19 patients, 9 were detected by mass screening sputum cytology studies and only one had an abnormal chest film. Thus, sputum cytology and mass screening can achieve the early detection of lung cancer, although the number of patients may be relatively small among the overall number of individuals undergoing screening. It should be noted that sputum cytology studies for the detection of lung cancer may sometimes show a falsepositive result. Martini et al. [3] pointed out that nearly 30% of patients with positive sputum cytology and clear chest films actually had cancer of head and neck origin. In our mass screening series, there were two patients who had a false-positive sputum cytology diagnosis of squamous cell carcinoma due to tongue cancer and laryngeal cancer, respectively. Bronchoscopic examination is a definitive test for such false-positive results, so that bronchofiberscopy combined with sputum cytology appears to be the ideal method of mass screening for early hilar cancer. In the symptomatic group, most of the patients had hemoptysis and/or cough. Bronchoscopy is crucially important in detecting early hilar lung cancer, since by definition the lesion is proximal to the segmental bronchus and will always be detected by a competent bronchoscopist. Small carcinomas in situ are sometimes very difficult to identify. Mucosal color changes, irregular capillaries, mucosal roughening, or thickening of the bronchial spur are the characteristic features of early hilar

A 4

5

6

+

A

h

10

years

Fig. 4. Survival curves of the 27 patients with early hilar lung cancer. Except for one patient who died of a second primary cancer in the 6th postoperative year, all the patients are still alive (100% 5-year survival and 91.7% 10-year survival).

cancer. In addition to the bronchoscopic appearance, brushing cytology and forceps biopsy of the suspicious lesions could allow a definitive diagnosis. The treatment modality selected in the present series was surgical resection of the lesion, excluding one synchronous in situ carcinoma which was cauterized using a YAG laser. This patient is doing well without any sign of recurrence 49 months after sleeve lobectomy and laser cauterization. Martini et al. [3] treated 47 patients with occult lung cancer and found that only the patient treated by excision had a long survival. In contrast, patients with presumed early disease treated by other means did poorly. For example, they treated one patient, who was thought to be unable to withstand lobectomy, by endoscopic cautery of a carcinoma in situ. The disease was controlled temporarily, but it has since recurred. It had been reported recently that endoscopic laser surgery could sometimes cure carcinoma in situ and superficially invasive tumors [10,11], but we followed a policy of aggressive surgical treatment for the lesions in the present series, including eight cases of carcinoma in situ. Limited bronchial resection was attempted whenever it was feasible and no patient underwent pneumonectomy, even when the lesion involved the main stem bronchus. Instead, sleeve lobectomy was performed in 15 patients, and standard lobectomy was used for the patients with lesions of the right middle and lower lobe bronchi or lesions of segmental bronchi. Two sleeve segmentectomies and one second carinal resection were performed for very small localized lesions. Local recurrence was not encountered in any of our patients. Furthermore, the pulmonary functions in the patients undergoing limited bronchial resection were satisfactorily preserved [ 121. When limited bronchial resection for bronchogenic carcinoma is performed, endoscopic observation and biopsy are crucial in delineating the extent

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of the disease and planning the site of resection, since this decision cannot be made by observing the outside of the involved bronchus at the time of operation. Martini et al. [9] reported that 38% of the patients with radiologically occult carcinoma developed a second primary carcinoma, and similar high incidence of second primary lesions in this particular group was reported by Cortese et al. [4,5]. Among the 27 patients in the present series, three patients (1 1.1%) developed second primary lung cancers. One patient had synchronous primary lesions which were treated by resection and laser surgery. One patient developed a metachronous second primary cancer of the opposite lung after the first sleeve lobectomy. This second early hilar cancer was successfully resected by another sleeve lobectomy, and the patient has achieved long-term survival. The last patient died of a second primary cancer after surviving over 5 years from the time of operation. As the incidence of the second primary cancer appears to be high in this group of patients, we are repeating sputum cytology studies and bronchoscopy every 6 months. In conclusion, the definition of early hilar lung cancer proposed by the JLCS seems to be reasonable from the clinical point of view. These lesions are curable if they are properly -diagnosed and treated. Mass screening of high risk individuals by sputum cytology and bronchoscopy can detect such lesions at the asymptomatic stage, while bronchoscopy is the best way to detect early hilar cancer in symptomatic patients. Surgery is the best treatment modality and parenchymal-sparing procedures should be selected as almost every patient will be a long-term survivor. The incidence of second primary cancer is high, and continuing bronchoscopic follow up is recommended for the early detection of second primary tumors.

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procedures for bronchial lesions. Ann Thorac Surg 50:607-6 14, 1990. Watanabe Y, Kobayashi H, Murakami S,Sawa S, Shinagawa M, Iwa T: Bilateral sleeve lobectomy for metachronous multiple primary lung cancer. Jpn J Surg 16:5&61, 1986. Martini N, Melamed MR: Occult carcinoma of the lung. Ann Thorac Surg 30:215-223, 1980. Cortese DA, Pairolero PC, Bergstralh EJ, Woolner LB, Uhlenhoop MA, Piehler JM, Sanderson DR, Bernatz PE, Williams DE, Taylor WF, Payne WS, Fontana RS: Roentogenologically occult lung cancer - a ten-year experience. J Thorac Cardiovasc Surg 861373-380, 1983. Woolner LB, Fontana RS, Cortese DA, Sanderson DR, Bemdtz PE, Payne WS, Pailorero PC, Piehler JM, Taylor WF: Roentogenologically occult cancer: pathological findings and frequency of multicentricity during a 10-year period. Mayo Clin Proc 59:453466, 1984. Payne WS, Bernatz PE, Pailolero PC, Piehler JM, Cortese DA, Fontana RS, Woolner LB: Localization and treatment of radiologically occult lung cancer. in Delarue NC, Eschapasse H (eds): “International Trend in General Thoracic Surgery. Vol. 1: Lung Cancer.” Philadelphia: W.B. Saunders Company, 1985, pp 8@87. Fontana RS, Sanderson DR, Taylor WF, Woolner LB, Miller WE, Muhm JR, Uhlenhopp MA: Early lung cancer detection: results of the initial (prevalence) screening in the Mayo Clinic study. Am Rev Respir Dis 130:561-565, 1984. Melamed MR, Flehinger BJ, Zamman MB, Heelan RT, Perchick WA, Martini N: Screening for early lung cancer. Results of the Memorial Sloan-Kettering study in New York. Chest 86:44-53, 1984. Martini N , Ghosn P, Melamed MR: Local recurrence and new primary carcinoma after resection. In Delarue NC, Eschapasse H (eds): “International Trend in General Thoracic Surgery. Vol. 1: Lung Cancer.” Philadelphia, W.B. Saunders Company, 1985, pp 164-169. Hayata Y, Kato H , Konaka C, Ono J, Takizawa N: Hematoporphyrin derivative and laser photoradiation in the treatment of lung cancer. Chest 81:269-277, 1982. Cortese DA, Kinsey JH: Hematoporphyrin derivative phototherapy in the treatment of bronchogenic carcinoma. Chest 86:8-13, 1984. Watanabe Y, Oda M, Shimizu J , Hayashi Y , Ohta Y, Iwa T, Tonami N, Hisada K: Functional advantage of parenchymalsparing surgery for early hilar lung cancer. Tohoku J Exp Med 163:135-148, 1991.

Early hilar lung cancer: its clinical aspect.

Early hilar lung cancers are rare, but are curable if they are properly diagnosed and treated. In the past 14 years, we have treated 27 patients with ...
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