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J Thorac Cardiovasc Surg 2004;128:396-401
© 2004 The American Association for Thoracic Surgery

General thoracic surgery

Fluorine 18–tagged fluorodeoxyglucose positron emission tomographic scanning to predict lymph node metastasis, invasiveness, or both, in clinical T1 N0 M0 lung adenocarcinoma

Hiroaki Nomori, MD, PhDa,*, Kenichi Watanabe, MDa, Takashi Ohtsuka, MDa, Tsuguo Naruke, MD, PhDa, Keiichi Suemasu, MD, PhDa, Toshiaki Kobayashi, MD, PhDb, Kimiichi Uno, MD, PhDc

a Department of Thoracic Surgery, Saiseikai Central Hospital, Tokyo, Japan
b Endoscopy Division, National Cancer Center Hospital, Tokyo, Japan
c Nishidai Clinic, Tokyo, Japan

Received for publication December 17, 2003; revisions received February 12, 2004; accepted for publication March 22, 2004.

* Address for reprints: Hiroaki Nomori, MD, PhD, Department of Thoracic Surgery, Saiseikai Central Hospital, 1-4-17 Mita, Minato-ku, Tokyo 108-0073, Japan
hnomori{at}qk9.so-net.ne.jp


   Abstract
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 Abstract
Materials and methods
 Results
 Discussion
 References
 
OBJECTIVE: We sought to predict lymph node metastasis and tumor invasiveness in clinical T1 N0 M0 lung adenocarcinomas, and we measured fluorodeoxyglucose uptake on positron emission tomography.

METHODS: Fluorodeoxyglucose positron emission tomography was performed on 44 patients with adenocarcinomas of 1 to 3 cm in size clinically staged as T1 N0 M0 before major lung resection with lymph node dissection. Fluorodeoxyglucose uptake was evaluated by using the contrast ratio between the tumor and contralateral healthy lung tissue. Lymphatic and vascular invasion within tumors, pleural involvement, and grade of histologic differentiation were examined.

RESULTS: The pathologic tumor stage was T1 N0 M0 in 36 patients, and a more advanced stage was found in 8 patients. Although all 22 adenocarcinomas with a contrast ratio of less than 0.5 in fluorodeoxyglucose uptake were pathologic T1 N0 M0 tumors, 8 (36%) of 22 with a contrast ratio of 0.5 or greater were of a more advanced stage than T1 N0 M0, with the difference being significant (P = .002). Adenocarcinomas with a contrast ratio of less than 0.5 showed less lymphatic and vascular invasion and less pleural involvement than those with a contrast ratio of 0.5 or greater (P = .006, P = .004, and P = .02, respectively). The grade of histologic differentiation was well differentiated in 19 of 22 adenocarcinomas with a contrast ratio of less than 0.5 (86%), which was a greater frequency than the 4 (18%) of 22 adenocarcinomas with a contrast ratio of 0.5 or greater (P < .001).

CONCLUSION: Clinical T1 N0 M0 lung adenocarcinomas with a contrast ratio of less than 0.5 usually did not have lymph node metastasis, had less tumor involvement of vessels or pleura, and were more frequently well differentiated than those with a contrast ratio of 0.5 or greater. Limited lung resection could be indicated, lymph node dissection or mediastinoscopy could be reduced, or both in this type of adenocarcinoma.


See related editorial on page 341.

 

Recent advances in low-dose helical computed tomography (CT) and video-assisted thoracoscopic surgery have enabled the diagnosis of lung cancers while still small in size.1-6 Although limited resection procedures, such as lung wedge resection or segmentectomy, can cure some clinical T1 N0 M0 non–small cell lung cancers (NSCLCs),7,8 lymph node metastases are still found in approximately 20% of clinical T1 N0 M0 lung adenocarcinomas.9-11 Even for patients with pathologic T1 N0 M0 NSCLCs, tumor involvement of intratumoral vessels or the pleura can also cause local recurrence after limited resection because of the spread of tumor cells into lymphatic vessels outside the primary tumor. To predict which T1 N0 M0 lung adenocarcinomas are curable with limited resection from CT findings, several reports have evaluated the importance of ground-glass opacity (GGO) within tumors, usually indicating bronchioloalveolar carcinoma–like spread because adenocarcinomas with GGO appearance are more frequently N0 stage and have less tumor involvement of intratumoral vessels or pleura than those with a solid appearance.12,13 The criteria of defining GGO appearance on CT scans are subjective, however, potentially leading to erroneous selection of limited surgical intervention.

In recent years, fluorodeoxyglucose (FDG) positron emission tomography (PET) has been used to evaluate pulmonary nodules and tumor stages. It has been reported that FDG uptake correlates with the proliferative activity of tumors14,15 and is an independent prognostic factor,16,17 particularly in lung adenocarcinoma. The prognosis in lung adenocarcinoma is known to depend on not only tumor stage but also tumor involvement of intratumoral vessels or pleura.9,10,18 To predict lymph node metastases and tumor involvement of intratumoral vessels or pleura in clinical T1 N0 M0 lung adenocarcinomas, we measured FDG uptake to determine any correlation with lymph node metastases, lymphatic and vascular invasion, and pleural involvement.


   Materials and methods
Top
 Abstract
 Materials and methods
Results
 Discussion
 References
 
Patients
From December 2001 through October 2003, prospective FDG-PET and CT scans were performed for 223 noncalcified pulmonary nodules. Of these, 93 nodules were malignant tumors less than 3 cm in diameter on CT. Clinical TNM stage was determined by using both CT and PET scanning. Of the 93 malignant nodules, 48 were clinical T1 N0 M0 adenocarcinomas of the lung, and these underwent major lung resection with mediastinal lymph node dissection. We excluded 4 adenocarcinomas less than 1 cm in diameter that were PET negative because the spatial resolution of the current generation of PET scanners is 0.7 to 0.8 cm, making it difficult to image pulmonary nodules of less than 1 cm. As a result, we studied 44 adenocarcinomas that were clinically staged as T1 N0 M0 of sizes from 1 to 3 cm. The medical record of each patient was examined with regard to age, sex, maximum tumor diameter, serum level of carcinoembryonic antigen (CEA; <5 ng/mL vs ≥5 ng/mL), operative procedure, pathologic TNM stage, vascular or lymphatic invasion within tumors (positive vs negative), pleural involvement (p0 vs p1 to p3), and grade of histologic differentiation. To identify tumor involvement of the intratumoral vessels or pleura, we routinely conducted elastica-van Gieson staining. Pleural involvement was classified as p0, p1, p2, or p3; that is, a p0 tumor did not extend beyond the elastic pleural layer, a p1 tumor invaded the visceral pleural elastic layer but did not reach the pleural surface, a p2 tumor included tumor exposure on the pleural surface, and a p3 tumor invaded the parietal pleura or chest wall. The tumor stages were based on the TNM classification of the International Union Against Cancer19: p2 tumors were classified as T2; p3 tumors were classified as T3; and tumors with intrapulmonary metastasis within the same lobe were classified as T4. Grades of histologic differentiation were classified as well, moderately, or poorly differentiated.

FDG-PET scanning
Patients were instructed to fast for at least 4 hours before intravenous administration of fluorine 18–tagged FDG. The dosage of fluorine 18–tagged FDG administered was 125 µCi/kg (4.6 MBq/kg) of body weight for nondiabetic patients and 150 µCi/kg (5.6 MBq/kg) of body weight for diabetic patients. PET imaging was performed approximately 60 minutes after administration of FDG with a POSICAM.HZL mPOWER (Positron Co, Houston, Tex). No-attenuation-corrected emission scans were initially obtained in 2-dimensional, high-sensitivity mode for 4 minutes per bed position and taken from the vertical skull through to the midthighs. Immediately thereafter, a 2-bed-position attenuation-corrected examination was performed, with 6 minutes for the emission sequence and 6 minutes for the transmission sequence at each bed position. The images were usually reconstructed in a 256 x 256 matrix by using ordered subset expectation maximization corresponding to a pixel size of 4 x 4 mm, with section spacing of 2.66 mm.

PET data analysis
The FDG-PET data were evaluated semiquantitatively on the basis of the contrast ratio (CR) obtained as follows. The regions of interest (ROIs) were placed in the nodules and contralateral lung. Highest activities in the tumor ROI (T) and in the contralateral normal lung ROI (N) were measured. The CR was calculated by using the formula (T – N)/(T + N) in each nodule as an index of FDG uptake. After correction for radioactive decay, the ROIs were also analyzed by computing the standard uptake value (SUV), which was calculated on the basis of the following equation: Tumor activity concentration/Injected dose/Body weight. The maximum SUV within the selected ROIs was also measured and compared with the results of CR.

Statistical analysis
All data were analyzed for significance by using the 2-tailed Student t test. All values in the text and tables are given as means ± SD.


   Results
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 Abstract
 Materials and methods
 Results
Discussion
 References
 
The pathologic tumor stage was T1 N0 M0 in 36 patients and more advanced in 8 patients (ie, T1 N1 M0 in 3 patients, T2 N0 M0 in 3 patients, and T4 N0 M0 in 2 patients). Lymphatic or vascular invasion within tumors and pleural involvement was seen in 19, 10, and 8 patients, respectively. Table 1 shows the various CR values with relation to the pathologic tumor stage, lymphatic and vascular invasion, and pleural involvement. Although all adenocarcinomas with a CR of less than 0.5 were pathologically staged as T1 N0 M0, some adenocarcinomas with a CR of 0.5 or greater were more advanced than T1 N0 M0, with more frequent lymphatic and vascular invasion and pleural involvement than the former. Therefore medical records were compared between the 22 adenocarcinomas with a CR of less than 0.5 and the 22 adenocarcinomas with a CR of 0.5 or greater.


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  		TABLE 1. Tumor involvements and pathologic TNM stage for each CR value

 
The maximum SUVs ranged from 0.5 to 3.1 (mean, 1.1 ± 0.7) in the 22 adenocarcinomas with a CR of less than 0.5 and from 1.9 to 8.5 (mean, 3.9 ± 1.8) in the 22 adenocarcinomas with CRs of 0.5 or greater, with the difference between the 2 groups being significant (P < .001). Two (9%) of the 22 adenocarcinomas with CRs of less than 0.5 showed an SUV of 2.5 or greater, however, both of which were pathologically staged as T1 N0 M0 and had no involvements of intratumoral vessels or pleura. Seven (32%) of the 22 adenocarcinomas with CRs of 0.5 or greater had SUVs of less than 2.5, of which 2 had a more advanced tumor stage than T1 N0 M0, 6 had lymphatic invasion, and 1 had vascular invasion.

Table 2 shows the results of PET findings with patients' characteristics, tumor size, and serum level of CEA. None of the adenocarcinomas with CRs of less than 0.5 had increased serum levels of CEA, which was significantly less frequent than the incidence of increased CEA in the 12 (55%) of 22 adenocarcinomas with CRs of 0.5 or greater (P < .001). There was no significant difference between the 2 groups in mean age, sex ratio, or tumor size.


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  		TABLE 2. PET findings and patients' characteristics, tumor size, and serum level of CEA

 
Table 3 shows the correlation between PET findings and pathologic tumor stage. All adenocarcinomas (100%) with CRs of less than 0.5 were staged as T1 N0 M0. Adenocarcinomas with CRs of 0.5 or greater were staged as T1 N0 M0 in 14 (64%) patients, T1 N1 M0 in 3 patients, T2 N0 M0 caused by p2 (tumor exposure on the pleural surface) in 3 patients, and T4 N0 M0 caused by intrapulmonary metastases in 2 patients. Adenocarcinomas with CRs of less than 0.5 were more likely to be pathologic T1 N0 M0 stage than those with CRs of 0.5 or greater (P = .002).


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  		TABLE 3. Correlation between PET findings and pathologic tumor stage

 
Table 4 shows the correlation between PET findings and lymphatic and vascular invasion within tumors and pleural involvement. Lymphatic invasion was seen in 5 (23%) of 22 adenocarcinomas with CRs of less than 0.5, which was significantly less frequent than 14 (64%) of 22 with CRs of 0.5 or greater (P = .006). Vascular invasion was seen in 1 (5%) of 22 adenocarcinomas with CRs of less than 0.5, which was significantly less frequent than 9 (41%) of 22 with CRs of 0.5 or greater (P = .004). Pleural involvement was seen in 1 (5%) of 22 adenocarcinomas with CRs of less than 0.5, which was significantly less frequent than 7 (32%) of 22 with CRs of 0.5 or greater (P = .02).


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  		TABLE 4. Correlation between PET findings and tumor involvement into intratumoral vessels or pleura

 
Table 5 shows the correlation between PET findings and the histologic degree of differentiation. In the adenocarcinomas with CRs of less than 0.5, well-differentiated and moderately differentiated adenocarcinomas were seen in 19 and 3 patients, respectively. In the adenocarcinomas with CRs of 0.5 or greater, well-differentiated, moderately differentiated, and poorly differentiated adenocarcinomas were seen in 4, 14, and 4 patients, respectively. Adenocarcinomas with CRs of less than 0.5 were more commonly well differentiated than those with CRs of 0.5 or greater (P < .001).


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  		TABLE 5. Correlation between PET findings and grade of histologic differentiation of adenocarcinomas

 
Table 6 shows the PET findings in well-differentiated adenocarcinomas with relation to the tumor stages and tumor involvements. Of the 4 well-differentiated adenocarcinomas with CRs of 0.5 or greater, each one (25%) was a pathologic T1 N1 M0 and T4 N0 M0 carcinoma, respectively; 4 (100%) had lymphatic invasion; 2 (50%) had vascular invasion; and 2 (50%) had pleural involvement. The well-differentiated adenocarcinomas with CRs of 0.5 or greater had advanced tumor stages, lymphatic and vascular invasion, and pleural involvement more frequently than those with CRs of less than 0.5 (P < .01, P < .001, P = .02, and P < .01, respectively).


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  		TABLE 6. Correlation between PET findings and tumor stages, tumor involvement of intratumoral vessels, and tumor involvement of pleura in well-differentiated adenocarcinomas

 

   Discussion
Top
 Abstract
 Materials and methods
 Results
 Discussion
References
 
Although a criterion for diagnosing pulmonary malignancy with FDG-PET has frequently used an SUV with a cutoff value of 2.5,20 some authors used visual evaluation, such as comparison of FDG uptake between nodules and mediastinal uptake.21 The present study evaluated FDG uptake with CR instead of SUV for the following reasons: (1)hyperglycemia in diabetic patients decreases both the blood clearance of FDG and the accumulation of FDG in tumor tissue, and (2) SUV could be different between fat and thin patients because it is measured by using a body weight. Actually, the mean SUV of malignant pulmonary nodules has been reported to be various, ranging from 5.5 to 10.1.22-25 In breast cancer, Wahl and coworkers26 have demonstrated that a CR between tumor and contralateral normal breast is a reliable indicator for diagnosing malignancy. We accordingly used CR in the present study and determined that the cutoff value to differentiate between aggressive and nonaggressive adenocarcinomas was 0.5, with which we could differentiate the degree of tumor aggressiveness more accurately than with SUV.

The important points of the present study are as follows. Compared with adenocarcinomas with CRs of 0.5 or greater, those with CRs of less than 0.5 (1) did not show an increased serum level of CEA, (2) did not have lymph node metastases, (3) had less tumor involvement of vessels or pleura, and (4) were more frequently well-differentiated adenocarcinomas. The serum level of CEA in lung adenocarcinomas has been reported to be higher in N1 or N2 disease than in N0 disease.27 FDG uptake in lung adenocarcinomas is known to often be negative in well-differentiated adenocarcinomas.28 It has been also reported that well-differentiated adenocarcinomas are more commonly N0 stage and have less tumor involvement of vessels or pleura than moderately or poorly differentiated lesions.9,12,13,18 Our results agree with those of these earlier studies. There were, however, 4 well-differentiated adenocarcinomas with CRs of 0.5 or greater that had more tumor aggressiveness than the 19 well-differentiated lesions with CRs of less than 0.5. We therefore consider that an FDG uptake on PET can predict lymph node metastases and tumor invasiveness more accurately than the grade of histologic differentiation in clinical T1 N0 M0 adenocarcinomas.

Although limited resection could be a reasonable approach for T1 N0 M0 lung cancers, it has been reported that lymph node metastases are found in about 20% of clinical T1 N0 M0 adenocarcinomas.9-11 In 1995, the Lung Cancer Study Group reported the results of a randomized control trial comparing limited resection and lobectomy for clinical T1 N0 M0 NSCLCs.29 This trial demonstrated the inferiority of limited resection in terms of local relapse and prognosis because some patients actually had pathologic N1 or N2 disease. This is also because tumor involvement of intratumoral vessels or the pleura can cause local recurrence after limited resection, even for pathologic N0 disease, because of the spread of tumor cells into lymphatic vessels outside the primary tumor.30 The present study showed that clinical T1 N0 M0 adenocarcinomas with CRs of less than 0.5 usually did not metastasize to the lymph nodes and seldom invaded the intratumoral vessels or pleura. This type of lung adenocarcinoma can be cured by means of limited surgical resection, such as segmentectomy or wedge resection. Although it has been reported that NSCLCs of less than 2 cm in size can be cured by means of segmentectomy with mediastinal lymph node dissection (ie, extended segmentectomy),7 the indication of the extended segmentectomy could be expanded for adenocarcinomas with CRs of less than 0.5 that are less than 3 cm in size.

Mediastinal lymph node dissection is a useful procedure to secure complete local control of an NSCLC, with a subsequent improvement in both survival and nodal staging.11 However, to minimize the damage caused by mediastinal node dissection in the patients with clinical stage I NSCLC, several authors reduced the dissection of some mediastinal lymph nodal stations with respect to the location of the primary tumor (ie, that the inferior and superior mediastinal lymph node stations could be reduced in the upper lobectomy and lower lobectomy, respectively).31,32 To expand the possibility of reduction of mediastinal lymph node dissection, a successful intraoperative sentinel lymph node biopsy has been reported.33,34 The present study showed that lymph node dissection could be reduced for clinical T1 N0 M0 adenocarcinomas with CRs of less than 0.5, without using the sentinel lymph node biopsy.

Although FDG-PET is well known to be useful for tumor staging in lung cancer, we believe that it can also predict lymph node metastases and tumor invasiveness in clinical T1 N0 M0 lung adenocarcinomas. Limited lung resection could be indicated, lymph node dissection or mediastinoscopy could be reduced, or both in this type of adenocarcinoma.


   Footnotes
 
This work was supported in part by a Grant-in-Aid from the Ministry of Health, Labor, and Welfare of Japan.


   References
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 Abstract
 Materials and methods
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 Discussion
 References
 

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