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J Thorac Cardiovasc Surg 1998;115:1015-1019
© 1998 Mosby, Inc.

GENERAL THORACIC SURGERY

Clinical analysis of small-sized peripheral lung cancer

Teruaki Koike, MDa, Masanori Terashima, MDa, Tsuneyo Takizawa, MDa, Takehiro Watanabe, MDa, Yuzo Kurita, MDb, Akira Yokoyama, MDb

From the Division of Chest Surgerya and the Division ofMedicine,b Niigata Cancer Center Hospital, Niigata, Japan.

Received for publication July 16, 1997. Revisions requested Oct. 14, 1997. Revisions received Dec. 15, 1997. Accepted for publication Dec. 15, 1997. Address for reprints: Teruaki Koike, MD, Division of Chest Surgery,Niigata Cancer Center Hospital, 2-15-3, Kawagishi-cho, Niigata 951, Japan.


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 References
 
Objective: In Japan, with the initiationof the lung cancer screening program, small-sized peripheral lung cancer inwhich the diameter is 2 cm or less has been increasing. The purpose of thisstudy is to determine the clinicopathologic behavior of small-sized lung cancer.
Methods: Four hundred ninety-six patientswith cT1 N0, peripheral, resected non-small-cell lung cancer, who were operatedon between 1980 and 1996, were selected, grouped by tumor diameter or histologictype, and then analyzed for clinicopathologic behavior. On the basis of measureddiameter roentgenographically, the patients were divided into two groups; groupc-S with lesions 2 cm or less in diameter and group c-L with lesions 2.1 to 3 cmin diameter.
Results: Lymph nodemetastasis was recognized in 18% of group c-S, in 23% of groupc-L, and in 21% for the entire clinical group. The rate of those with theprogressive state was 19% in group c-S and 26% in group c-L. The5-year survival was 79.5% in group c-S and 69.3% in group c-L(i.e., there was a significant difference between the two groups).
Conclusion: Compared with the patients with lesions 2.1 to3 cm in diameter, the patients with small-sized lung cancer had a milderprogressive state and a better prognosis.(J Thorac Cardiovasc Surg1998;115:1015-20)


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 References
 
Recently in Japan, with the spread of mass screening for lung cancer,there have been many opportunities to resect small-sized peripheral lung cancerswith diameters of 2 cm or less. Occasionally it is difficult to decide whetherwe should perform lobectomy or add systematic lymphadenectomy in patients withsmall-sized lung cancers. As these small-sized lung cancers increase, however,it becomes important to consider the clinicopathologic behavior of these tumorsand to determine an optimal treatment strategy. In our institute, patients withlung cancer have usually been treated with lobectomy and added systematiclymphadenectomy, and recently we began to apply limited resection to a fewpatients with small-sized lung cancer. Thus we can reliably detect theintrathoracic pathologic spread of these small-sized lung cancers. The purposeof this study is to determine the clinicopathologic behavior of small-sized lungcancer retrospectively.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 References
 
After the introduction of chest computed tomographic scanning forpreoperative clinical staging, patients with resected primary lung cancertreated at our institution from January 1980 to December 1996 were the subjectsof this study. The following criteria were used. Peripheral cT1 N0 M0 lungcancer with a maximum diameter of 3 cm or less, measured on plain chest x-rayfilms or computed tomographic scans, were the first criterion. The staging oflung cancer was based on the TNM classification of the Union InternationalCancer Conference.Go 1 Thesecond criterion was that the patients had no former treatment. The thirdcriterion was that the histologic type be non-small-cell lung cancer, exceptsmall-cell lung cancer or low-grade malignant tumors. The fourth criterion wasthat lobectomy had been performed with complete hilar and mediastinallymphadenectomy. A total of 496 patients were selected, 255 of whom were men and241 were women. They ranged in age from 29 to 83 years (mean age 63 years). Theselected patients were separated clinically into two subgroups by tumordiameter; the small group (group c-S) consisted of patients in whom the tumordiameter measured on plain chest x-ray films or by computed tomographic scanningwas 2 cm or less, and the large group (group c-L) consisted of patients in whichthe diameter was 2.1 to 3 cm. The patients were classified into another twosubgroups based on the resected tumor diameter; the postoperative small group(group p-S) consisted of patients with tumors 2 cm or less in diameter, and thepostoperative large group (group p-L) consisted of patients with tumors 2.1 to 3cm in diameter (Fig. 1). Among 225 group c-S patients, 149 (66%)in whom the resected tumor diameter was 2 cm or less were classified as groupp-S, and in 271 group c-L patients, 156 (58%) in whom the resected tumordiameter was 2.1 to 3 cm were classified into group p-L. Three hundred fivepatients (61%) showed a match between clinical diameter and postopertivediameter, 54 patients (11%) overestimation, and 137 patients (28%)underestimation.



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  		Fig. 1. Schema of clinical andpostoperative groups. Group c-S consisted of cases with a maximum tumor diameteras measured by roentgenography or computed tomography of 2 cm or less. Group c-Lconsisted of cases with a roentgenographic tumor diameter of 2.1 to 3 cm. Groupp-S consisted of cases in which the resected specimen diameters were 2 cm orless, and group p-L consisted of cases in which the resected specimen diameterswere 2.1 to 3 cm.

 
Statistical analysis was carried out using the {chi}2 test.Survival was calculated by the Kaplan-Meier life-table method and compared withthe generalized Wilcoxon test. Multivariance analysis of the prognostic factorswas conducted by Cox's regression model. It was performed with SAS software (SASInstitute, Inc. Cary, N.C.).


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 References
 
When the tumor cell cytologic findings were judged to be class IV or V,lung cancer was diagnosed. In 90% of the patients, lung cancer wasdiagnosed before the operation (Table I).The positive rate was 92% in group c-L and 87% in group c-S,showing a decrease with the reduction in tumor diameter. At our institution, toobtain tumor cells, we first examined patients with a flexible fiberopticbronchoscope. If no positive tumor cells were obtained, we attemptedpercutaneous needle biopsy. Eighty-one percent of cases were diagnosed byexamination with fiberoptic bronchoscopy and 9% by needle biopsy. Thepositive rate by needle biopsy in group c-S was higher than that in group c-L.Thus for small-sized lung cancer the needle biopsy examination appears toincrease the positive rate.


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  		Table I. Preoperative diagnosis:clinical group
 
According to the classification by pathologic staging, p stage I was 82%in group c-S and 74% in group c-L (Table II).The rate of p stage I in group c-S was higher than in group c-L. This tendencywas also seen in the postoperative group; p stage I was 83% in group p-Sand 76% in group p-L.


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  		Table II. Pathologic stage according totumor diameter
 
Lymph node metastasis was recognized histologically in 18% ofgroup c-S, 23% of group c-L, and 21% of the entire clinical group,whereas intrapulmonary metastasis was recognized in 1% of group c-S, 2%of group c-L, and 2% of the clinical group (Table III).Pleural dissemination or malignant effusion was recognized histologically in 1%of group c-S, 3% of group c-L, and 2% of the clinical group. Ifthere are certain progressive conditions, such as lymph node metastasis,intrapulmonary metastasis, pleural dissemination, or malignant effusion, limitedresection increases the risk of incomplete resection. Among 225 group c-Spatients, lymph node metastasis alone was recognized in 38 patients,intrapulmonary metastasis alone in 1 patient, and malignant effusion alone in 2patients. Lymph node metastasis and intrapulmonary metastasis were recognizedconcurrently in one patient, and lymph node metastasis and malignant effusionwere found concurrently in one patient. Therefore the risk of incompleteresection was suspected to be approximately 19% in group c-S and 26%in group c-L. The same tendency was seen in postoperative tumor diameter. Theincidence rates of lymph node metastasis, intrapulmonary metastasis, pleuraldissemination, and malignant effusion in group p-L were higher than those ingroup p-S. Thus the risk of incomplete resection in p-L was higher than that inp-S.


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  		Table III. Pathologic confirmationaccording to tumor diameter
 
In the clinical group, according to the classification of histologictypes, lymph node metastasis was recognized in 11% of squamous cellcarcinoma, 22% of adenocarcinoma, and 40% of other cell types(five patients had large cell carcinoma and five patients had adenosquamous cellcarcinoma) (Table IV).Intrapulmonary metastasis was recognized in only 2% of patients withadenocarcinoma, pleural dissemination or malignant effusion in only 3% ofthese patients. The risk of incomplete resection was 11% in squamous cellcarcinoma, 24% in adenocarcinoma, with the risk rate in adenocarcinomasignificantly higher than that in squamous cell carcinoma (p =0.02).


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  		Table IV. Pathologic confirmationaccording to histologic type
 
In the other subgroups of the clinical group, rates were the same as inthe postoperative group. In the postoperative group, lymph node metastasis wasrecognized in 10% of squamous cell carcinoma, 24% ofadenocarcinoma, and 2% each of intrapulmonary metastasis and pleuraldissemination or malignant effusion with adenocarcinoma. The risk of incompleteresection was 10% for squamous cell carcinoma and 22% foradenocarcinoma.

In the subgroups classified by histologic type and tumor size, the rateof lymph node metastasis of adenocarcinoma was higher than that of squamous cellcarcinoma in both the clinical and the postoperative group (Table V).For adenocarcinoma, the positive rate of group c-S was lower than thatof group c-L, and the positive rate of group p-S was lower than that of groupp-L. Rates were, however, variable in the postoperative group, with threepositive cases in group c-L showing a change in diameter postoperatively. Twopatients shifted to group p-S, and one patient shifted to the more than 3 cm indiameter group. Thus the positive rate of group p-S was higher than that ofgroup p-L.


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  		Table V. Lymph node metastasis accordingto tumor diameter and histologic type
 
In squamous cell carcinoma no intrapulmonary metastasis, dissemination,or malignant effusion was recognized, such that the risk rate for incompleteresection was the same as that of lymph node metastasis (Table VI).In every group the risk rate for incomplete resection in adenocarcinoma washigher than that of squamous cell carcinoma, whereas the risk rate of squamouscell carcinoma in group c-S was significantly lower than that of adenocarcinomain group c-L (p = 0.03).


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  		Table VI. Risk of incomplete resectionaccording to tumor diameter and histologic type
 
Postoperative survivals were calculated with the inclusion of all deaths.The 5-year survival was 79.5% in group c-S, 69.3% in group c-L,79.2% in group p-S and 70.4% in group p-L (Fig. 2). The survival curve of group c-S wassignificantly higher than that of group c-L (p =0.02), and the survival curve of group p-S was higher than that of group p-L (p = 0.04). Results of multivariative analysis of theprognostic factors are shown in Table VII. Theexistence of risk factors is significant and tumor size is not. Excludingpatients with risk factors, 5-year survival was 79.8% in group p-L (n = 170), 88.9% in group p-S (n = 166), and the survival curve of group p-S wassignificantly higher than that of group p-L (p =0.01).



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  		Fig. 2. Postoperative survivalcurve. The survival curve of group c-S was significantly higher than that ofgroup c-L (p = 0.02), and the survivalcurve of group p-S was higher than that of group p-L (p =0.04).

 

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  		Table VII. Multivariate analysis ofprognostic factors
 

   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
References
 
In 1987 the Japanese Ministry of Health and Welfare decided to includelung cancer screening with plain chest x-ray films and sputum cytologicexamination as one of the cancer screening programs provided by the Health andMedical Services Law for the Aged. With the spread of this program,identification of patients with peripheral small-sized lung cancer with adiameter of 2 cm or less has been increasing. However, it is not easy todiagnose these small-sized lung cancers in the preoperative period. In thereports by Cortese and McDougallGo 2and Stringfield and coworkers,Go 3the cytologic positive rate by bronchoscopy in peripheral small-sized lungcancer was low (i.e., less than 50%). Mori and coworkersGo 4 reported that they detected 68%of these cases, 66% by a fiberoptic bronchoscope and 2% by needlebiopsy. In our institution we were able to diagnose 87% of small-sizedlung cancers, with 12% detected by percutaneous needle biopsy. Thus it isuseful to conduct percutaneous needle biopsy for these small-sized lung cancers.

In all our patients with lung cancer, clinical staging was doneroentgenographically, with plain chest x-ray films and computed tomographicscanning, before the operation. The patients with tumors estimated to be cT1 N0M0, stage I preoperatively and judged pathologically to be stage I accounted foronly 78%; those estimated to be peripheral small-sized cT1 N0 M0preoperatively and judged pathologically to be stage I accounted for 82%.The major cause of changes in pathologic staging was the existence of lymph nodemetastasis.

The focus of this study was cT1 N0 M0 peripheral non-small-cell lungcancer. Lymph node metastasis was recognized in 21% of tumors 3 cm orless on the basis of roentgenographic size and in 20% of tumors 3 cm orless measured postoperatively. Asamura and coworkersGo 5 reported the lymph node metastasisrate to be 22% in cN0 non-small-cell lung cancers 3 cm or less, andTateishi and coworkersGo 6reported the metastasis rate to be 30% in any cN non-small-lung cancers 3cm or less. Therefore it was suspected that lymph node metastasis of cT1 N0 M0,peripheral, non-small-cell lung cancer was approximately 20%. Comparingtumors 2 cm or less with those 2.1 to 3 cm, the metastasis rate was 20%in the former and 33% in the latter.Go 5Ishida and coworkersGo 7reported that the metastasis rate was 15% for tumors 2 cm or less and 38%for those in 2.1 to 3 cm. Among our patients the metastasis rate was 17%or 18% for patients with small-sized lung cancers and 23% forthose with tumors 2.1 to 3 cm, but the difference between the two groups did notreach statistical significance.

According to histologic type, among the patients with any cN 3 cm orless, Asamura and coworkersGo 5reported the lymph node metastasis rate to be 17% in adenocarcinoma and14% in squamous cell carcinoma. In our study, among the patients with cN03 cm or less, the metastasis rate was 22% in adenocarcinoma and 11%in squamous cell carcinoma. Among the patients with tumors 2 cm or less, Asamuraand coworkersGo 5 reported thatthe metastasis rate was 11% in adenocarcinoma and 6% in squamouscell carcinoma. The corresponding rates in our series were 17% and 15%.Thus the lymph node metastasis rate of squamous cell carcinoma was lower thanthat of adenocarcinoma.

Intrapulmonary metastasis existed in 1% to 2%, and pleuraldissemination or malignant effusion was recognized in 1% to 3%. Inthose with lymph node metastasis, pulmonary metastasis, pleural dissemination,or malignant effusion, limited resection is not appropriate. The risk rate forincomplete resection was predicted to be 18% to 19% in small-sizedlung cancer and 21% to 23% with 2.1 to 3 cm tumors. Furthermore,according to histologic type, there was a low incidence of squamous cellcarcinoma.

Comparing the survival rate of the group with tumors 2 cm or less indiameter with that of the group whose tumors were 2.1 to 3 cm in diameter,Asamura and coworkersGo 5reported that there was no difference between the two groups in those withoutlymph node metastasis. In our study, however, there were significant differencesbetween the two groups. Recently, MottaGo 8reported in a review describing the current state in Europe that there was adefinitive difference in postoperative survival between pT1 N0 and pT2 N0. Itwas therefore suspected that the postoperative survival with small-sized lungcancer was better than that associated with tumors 2.1 to 3 cm in diameter.There have been several reportsGo Go Go 7,9,10indicating that the survival of patients with small-sized lung cancer was betterthan that of those with 2.1 to 3 cm tumors. The 5-year survival of the 84patients with 1.1 to 2 cm diameter tumors was 74% and was thus betterthan that of 129 patients with 2.1 to 3 cm cancers reported by Ishida andcoworkers.Go 7 Read andcoworkersGo 9 reported thatamong T1 N0 cases undergoing several different operative procedures, thesurvival of 146 patients with tumors 2 cm or less was significantly better thanthat of 98 patients with tumors 2 cm or more. Warren and coworkersGo 10 reported that the survival ofpatients with cancers 2 cm or less was better than those with tumors 2.1 to 3cm. Thus it is our view that among T1 N0 cases, the survival of patients withsmall-sized lung cancer (i.e., a diameter of 2 cm or less) is better than thatof other T1 N0 cases.

In conclusion, in the cT1 N0 group, non-small cell lung cancer, lymphnode metastasis was recognized in 21% and there was a possibility ofprogressive disease in 23%. With small-sized lung cancers having adiameter of 2 cm or less, lymph node metastasis was recognized in 18%,and the possibility of progressive disease in 19%. According tohistologic findings, squamous cell carcinoma had a lower rate of lymph nodemetastasis and was less often a progressive disease than adenocarcinoma.


   Footnotes
 
Consultant statistician: Koichi Inada, DSc, Department of Mathematics and Computer Science, Faculty of Science, Kagoshima University, Kagoshima 890, Japan.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

  1. Mountain CF. A new international stagingsystem for lung cancer. Chest 1986;89:225s-33s.
  2. Cortese DA, McDougall JC. Biopsy andbrushing of peripheral lung cancer with fluoroscopic guidance. Chest 1979;75:141-5.[Abstract/Free Full Text]
  3. Stringfield JT, Markowitz DJ, Bentz RR,Welch MH, Weg JG. The effect of tumor size and location on diagnosis byfiberoptic bronchoscopy. Chest 1977;72:474-6.[Abstract/Free Full Text]
  4. Mori K, Yanase N, Kaneko M, Ono R, Ikeda S.Diagnosis of peripheral lung cancer in cases of tumors 2 cm or less in size.Chest 1989;95:304-8.[Abstract/Free Full Text]
  5. Asamura H, Nakayama H, Kondo H, Tsuchiya R,Shimosato Y, Naruke T. Lymph node involvement, recurrence, and prognosis inresected small, peripheral, non-small-cell lung carcinomas. J ThoracCardiovasc Surg 1996;111:1125-34.[Abstract/Free Full Text]
  6. Tateishi M, Fukuyama Y, Hamatake M, KohdonoS, Mitsudomi T, Ishida T, et al. Characteristics of non-small cell lung cancer 3cm or less in diameter. J Surg Oncol 1995;59:251-4.[Medline]
  7. Ishida T, Yano T, Maeda K, Kaneko S,Tateishi M, Sugimachi K. Strategy for lymphadenectomy in lung cancer threecentimeters or less in diameter. Ann Thorac Surg 1990;50:708-13.[Abstract]
  8. Motta G. Recent advances in lung cancersurgery in Europe. Lung Cancer 1996;16:1-11.[Medline]
  9. Read RC, Yoder G, Schaeffer RC. Survivalafter conservative resection for T1 N0 M0 non-small cell lung cancer. Ann ThoracSurg 1990;49:391-400.[Abstract]
  10. Warren WH, Faber LP. Segmentectomy versuslobectomy in patients with stage I pulmonary carcinoma. J Thorac CardiovascSurg 1994;107:1087-94.



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E. F. Patz Jr., S. Rossi, D. H. Harpole Jr., J. E. Herndon, and P. C. Goodman
Correlation of Tumor Size and Survival in Patients With Stage IA Non-small Cell Lung Cancer
Chest, June 1, 2000; 117(6): 1568 - 1571.
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