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© 2003 European Association of Cardio-Thoracic Surgery
Bronchoscopically undiagnosed small peripheral lung tumors
a Division of Surgery, Toneyama National Hospital, 5-5-1 Toneyama, Toyonaka, Osaka 560-8552, Japan
* Corresponding author. Tel.:+81-6-6853-2001; fax:+81-6-6850-1750 Received December 9, 2002; received in revised form February 26, 2003; accepted April 11, 2003
Small peripheral lung cancers (2 cm or less maximum diameter) are often surgically resected, and the survival rate of those patients has been reported to be significantly higher than that of patients with tumors 2.1 cm or more in diameter. We evaluated the status of these small tumors diagnosed during surgery, following unsuccessful transbronchial biopsy procedures. In a retrospective study, 84 consecutive patients, with a maximum diameter of 2 cm or less on chest computed tomography, were enrolled. All underwent surgery for diagnosis. Video-assisted thoracoscopic surgery was performed in 49 cases (58%), Video-assisted thoracoscopic surgery+mini-thoracotomy in ten cases (12%), and an open lung biopsy in 25 cases (30%). Primary lung cancer was found in 40 cases (48%), metastatic lung tumors in three cases (3%), and benign lung tumors in 41 cases (49%). Among the 40 primary lung cancer cases, adenocarcinoma was in 38, squamous cell carcinoma was in one, and small cell carcinoma was in one. The rate of stage IA was 90%. Surgical excision of undiagnosed small peripheral nodules without waiting is necessary if transbronchial biopsy diagnosis is unsuccessful, because of the high rate of stage IA non-small cell lung cancer.
Key Words: Lung cancer; Excision; Video-assisted thoracoscopic surgery; Transbronchial biopsy; Computed tomography-guided fine-needle aspiration cytology
Small peripheral lung cancers (2 cm or less maximum diameter) are often surgically resected [1], and the survival rate of those patients has been reported to be significantly higher than that of patients with tumors 2.1 cm or more in diameter [1]. However, techniques such as transbronchial biopsy and computed tomography-guided fine-needle aspiration cytology are limited in their ability to diagnose such small lung tumors [1,2]. Lung cancers should be diagnosed as early as possible in order for the patient to have the best opportunity to recover from the disease. Those detected using thoracotomy or Video-assisted thoracoscopic surgery (VATS) have been reported to be more frequently diagnosed as Stage IA than those by the use of transbronchial biopsy [3]. As a result, we have been performing surgical procedures for the diagnosis of small lung tumors that are highly suspicious from the CT findings. Herein we report the results of a retrospective study using consecutive patients to assess the effectiveness of our surgical strategy for diagnosis of indeterminate small peripheral tumors and evaluate the potential malignancy within these indeterminate tumors.
Eighty-four consecutive patients, 37 men and 47 women, with a mean age of 56.0 years (range 27–77 years), who had small peripheral lung tumors 2 cm or less in diameter on chest CT were treated between January 2000 and September 2001 at Toneyama National Hospital, Japan, after giving informed consent. All were attempted to undergo transbronchial biopsy, and four patients also underwent computed tomography-guided fine-needle aspiration cytology. They underwent a surgical procedure for diagnosis, which was surgical excision soon after unsuccessful transbronchial biopsies or refusals of patients to transbronchial biopsy. Reasons for selecting surgery are shown in Table 1, of which the most frequent was difficulty in diagnosis using transbronchial biopsy.
VATS exploration was given priority for tumors located within 3 cm of the visceral pleura, while open lung biopsy was preferred for the others. Further, if a tumor shadow showed dominant gland glass attenuation (GGA), defined as a hazy increased attenuation of the lung with bronchial and vascular structures in the lesion, in the CT image [4], a surgical diagnostic procedure was performed after a follow-up within 3 months. Even in such GGA cases, transbronchial biopsy was also performed.
Among the 84 lesions studied, 43 (51%) were detected by lung cancer screening, 31 (37%) during a follow-up examination for other diseases, and ten (12%) from symptoms. Further, 53 lesions (63%) were detected by chest roentgenogram and 31 (37%) only by chest CT. The tumor diameters, as measured by chest CT, ranged from 5 to 20 mm with a mean of 13.1 mm (Table 2). Those 10 mm or less were found in 35 cases (42%). The location and CT findings of these lung tumors are shown in Table 2. VATS exploration was performed in 49 cases (58%), VATS+mini-thoracotomy in ten cases (12%), and open lung biopsy in 25 cases (30%). VATS explorations were intended to determine histology by wedge resection; however, two cases underwent VATS needle aspiration biopsy. Such cases of VATS+mini-thoracotomy and open lung biopsy were selected due to severe adhesion or difficulty in detecting tumors. The resected specimens were diagnosed using frozen sections when the tumor was diagnosed to be a non-small cell lung cancer, and further pulmonary resections were undertaken subsequently if appropriate.
Pathological diagnoses for the 84 lesions are shown in Table 3. Among them, 43 (51%) were diagnosed as a malignant lung tumor and 41 (49%) as benign (Table 3). Among the 43 malignant lung tumors, primary lung cancer was found in 40 cases and metastatic lung tumor in three cases. Histological diagnosis of the 40 primary lung cancers were adenocarcinoma in 38 cases, and one case each of squamous cell carcinoma and small cell carcinoma. There was a single case of false-negative malignancy, in which the diagnosis after examining the frozen section was organizing pneumonitis and difficult to differentiate from malignancy. The surgical intervention procedures used for primary lung cancers were shown in Table 4; lobectomy was in 28 cases, segmentectomy in three cases, and wedge resection in nine cases. Among these latter nine cases, bronchioloalveolar carcinoma was found in eight cases and small cell carcinoma in one. The pathological stage was IA in 27 cases, IIIA in one case, IIIB in one case due to malignant pleural effusion, and IV due to pulmonary metastasis in two cases, while N factors were not diagnosed in nine cases that had a wedge resection (Table 4). All lesions were completely resected grossly; however, two cases had pulmonary metastasis. In every case, the postoperative course was uneventful.
There are various noninvasive and minimally invasive diagnostic procedures available for the evaluation of indeterminate solitary pulmonary lesions, among which transbronchial biopsy and computed tomography-guided fine-needle aspiration cytology are the most important for lung cancer [5,6]. Transbronchial biopsy is routinely given the highest priority for lung tumors, while computed tomography-guided fine-needle aspiration cytology is preferred for peripheral lesions if a diagnosis cannot be determined by transbronchial biopsy. However, it is sometimes difficult to diagnose small peripheral lung cancerous lesions that are 2 cm or less in diameter using only these procedures [2]. Moreover, lung cancer diagnosed by transbronchial biopsy alone is frequently in an advanced stage, because of the higher grade of central fibrosis, regardless of tumor size [3]. At our institution, transbronchial biopsy has a higher priority than computed tomography-guided fine-needle aspiration cytology, as the latter has the potential to spread malignant cells from the tumor to the pleural space [7], though transpleural techniques do not affect relapse and prognosis [8]. Charig et al. [9] reported that 66% of patients with no malignant cells found by transbronchial biopsy and without a definite benign diagnosis actually had malignancy. As a result, when malignancy is not positively identified by transbronchial biopsy, they are likely to choose thoracotomy to establish an accurate diagnosis. VATS exploration methods have been documented to be both minimally invasive and very useful [10–12], and have been shown to detect early-stage lung cancer as well as thoracotomy more frequently than transbronchial biopsy procedures [3]. Generally lung cancers are not detected until they have reached an advanced stage, thus, even if radical surgery is undertaken, the survival rate is poor [6]. Postoperative survival of patients with small peripheral lung tumors 2 cm or less in diameter was better than those associated with lesions 2.1–3 cm in diameter [1]. Therefore, diagnosis before the advanced stage is critical, and delays before evaluation and operation can be reduced to improve the survival rate by employing an invasive diagnostic procedure such as surgery. Bronchioloalveolar carcinoma appears to be increasing in incidence in lung adenocarcinoma, and it was recently reported that localized pure bronchioloalveolar carcinoma had a good prognosis without nodal involvement [13]. Among our 38 adenocarcinomas, 22, including 19 bronchioloalveolar carcinomas, were detected only by chest CT. And therefore, CT screening may be useful to detect early-stage lung cancer. Reasons for our selecting incomplete resections are due to the histologic type A or B using Noguchi's classification, multiple GGA, pulmonary metastasis, and severe complications such as emphysema. Over the past several years, positive emission tomography (PET) has become an important imaging modality in both the diagnosis and staging of lung cancer [14,15]. However, false negatives can occur in association with bronchioloalveolar carcinomas, carcinoids, and in tumors less than 10 mm in diameter [14,15]. On the contrary, false positives are related to inflammatory lesions such as tuberculoma, abscess, sarcoidosis [15]. PET may remain to be limited in its ability to detect those tumors, such as in our study. In conclusion, our investigation revealed that more than half of the indeterminate small lung lesions that could not be diagnosed using transbronchial biopsy were malignant and nearly all were stage IA non-small cell lung cancer. Therefore, we consider that surgical diagnosis following CT screening is warranted to detect and cure early-stage lung cancer.
ICVTS on-line discussion Author: H.V. Rajashekara Reddy, Specialist Registrar, Norfolk & Norwich University Hospital, Department of Thoracic Surgery, Norwich, UK Date: 29-Jul-2003 Message: This Institutional Review again shows the importance of the need for definite histology, unsurprisingly given the growing number of possibilities. May I ask for these clarifications: 1. Since transbronchial biopsy, in about 85% (72/84) of the cases, is not achieving diagnosis in the majority, should we go directly for surgery. 2. In the discussion the authors say "PET may remain to be limited in its ability to detect those tumours, such as in our study". I don't think the authors have given their figures of PET scan in the series of patients, with 49/84 (58%) of them having lesions of more than 10 mm size. Does the size correlate with histology? Response Author: Dr. Yasunobu Funakoshi, Toneyama National Hospital, Department of Surgery, 5-5-1 Toneyama, Toyonaka, 560-8552 Japan Date: 11-Aug-2003 Message: 1. In western countries, VATS excision is preferred to transbronchial biopsy from the cost-effective point of view. In Japan, the cost-effectiveness of diagnostic procedures is different from that in western countries. Transbronchial biopsy is the lowest-cost diagnostic procedure. Therefore, in Japan, this procedure is often performed prior to VATS excision. However, we think that transbronchial biopsy is not effective for most gland glass attenuation cases. As you detect, for such tumors, we should perform VATS excision directly. 2. In the majority of our series, PET scans are not evaluated. In Japan, PET scan is the highest-cost imaging modality. Among 28 tumors with 1.1–1.5cm in diameter, malignant tumor was found in 20 cases (71%), including 9 bronchioloalveolar carcinomas, tuberculoma in 6 cases, and sarcoidosis in one case. Among 21 tumors with 1.6–2.0cm, malignant tumor was found in 12 cases (57%) and tuberculoma in 3 cases. PET scans may avoid the unnecessary invasiveness in patients with benign nodules more than 1.1 cm. Our conclusion is that VATS excision is the sensitive diagnostic modality for indeterminate small peripheral lung nodules.
Presented at the American College of Chest Physicians Annual Meeting (CHEST 2002), San Diego, CA, USA on November 6, 2002. doi:10.1016/S1569-9293(03)00078-1
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Abstract
1. Introduction
