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Ann Thorac Surg 2004;77:415-420
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Optimal distance of malignant negative margin in excision of nonsmall cell lung cancer: a multicenter prospective study

Noriyoshi Sawabata, MDa,b*, Mitsunori Ohta, MDa, Akihide Matsumura, MDa,c, Katsuhiro Nakagawa, MDa,d, Hiroshi Hirano, MDe,f, Hajime Maeda, MDa,b, Hikaru Matsuda, MD, PhDa Thoracic Surgery Study Group of Osaka University

a Division of General Thoracic Surgery, Department of Surgery (E-1), Osaka University, Graduate School of Medicine, Toyonaka, Osaka, Japan
b Division of Surgery, Suita, Japan
f Toneyama National Hospital, Toyonaka, Osaka, Japan
c Division of Surgery, National Kinki-Chuo Hospital for Chest Diseases, Sakai, Japan
d Division of Surgery, Habikino Hospital, Habikino, Japan
e Department of Pathology, Hyogo College of Medicine, Nishinomiya, Japan

Accepted for publication August 1, 2003.

* Address reprint requests to Dr Sawabata, Division of Surgery, Toneyama National Hospital, 5-1-1 Toneyama, Toyonaka, Osaka 560-8552, Japan
e-mail: nsawabata{at}m5.dion.ne.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Complete excision of nonsmall cell lung cancer is necessary during a limited resection procedure, as a malignant positive margin can lead to margin relapse. Because there is scant information available regarding the optimal size of a malignant negative margin, we conducted a multicenter, prospective study to more fully elucidate this area of concern.

METHODS: Two hundred five pulmonary tumors (22 nonsmall cell lung cancers and 183 undiagnosed lesions) were excised, of which 118 nonsmall cell lung cancer lesions were analyzed. Malignant status was considered positive when either a cytologic or histologic technique revealed the margin to be malignant. Maximum tumor diameter (from 4 to 45 mm with an average of 15.3 mm), margin distance (from 0 to 25 mm with an average of 9.3 mm), tumor location, extent of stapling carried out, and performance of a thoracotomy were the variables.

RESULTS: Seventy-two of the sample tissues (61%) were malignant negative. The negative group had smaller maximum tumor diameter, greater margin distance, lesions in more easily resectable regions, and more often required stapling only. Using a multivariate analysis, maximum tumor diameter and margin distance were found to be independent factors. The number of malignant negative margins was 7/7 (100%) when the margin distance was greater than 20 mm, and the number of malignant negative margins was 21 of 21 (100%) when the resected tumors had a margin distance greater than the maximum tumor diameter.

CONCLUSIONS: Malignant positive margins were not found when the margin distance was greater than the maximum tumor diameter, which was considered to be the optimal margin distance for prevention against margin relapse.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
A limited pulmonary resection for nonsmall cell lung cancer (NSCLC) has two indications: (1) an intentional limited resection and (2) a compromised limited resection. In the former, a segmentectomy is an option, which is generally carried out for small peripheral lesions (less than 2 cm maximum diameter) and has a similar survival rate as a lobectomy [1, 2]. A wedge resection can also be used for an intentional, limited resection and is usually carried out for lesions with a diminutive malignant potential (eg, bronchiolo-alveolar cell carcinoma)[3, 4]. As for a compromised limited resection, a wedge resection is one of the most common techniques to remove NSCLC tumors from high-risk patients [5–8].

An NSCLC lesion should be resected appropriately, as a malignant positive margin has the potential to cause surgical margin relapse [5–11]. It has been shown that cytologically malignant positive margins cause margin relapse in 40% to 60% of such cases, even if the resected malignant tumor has a negative histology margin [12–15].

A large amount of distance between the surgical margin and tumor can provide a malignant negative margin; however, it is sometimes very difficult to obtain, because the amount of lung tissue that is removable is limited. We conducted a multicenter, prospective study in order to determine the distance threshold for a malignant negative surgical margin for excision of NSCLC using both compromised patients and good-risk patients who underwent a completion lobectomy.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Study design
We recently developed a new technique (the run-across method) that is used to extract tissue samples from the whole of the surgical margin. An explanation of this technique and preliminary results were first published in 1999 [12]. In that study we found that approximately half of the surgical margins contained malignant cells, which have a potential to cause relapse. Following that report, we established a protocol for our technique and carried out a multicenter study, which has been reviewed by a local institution review board. The protocol states that the selection criteria for a high-risk patient is clinical stage I, which is diagnosed using a chest computed tomographic scan, brain magnetic resonance image, an abdominal computed tomographic scan, and a bone scintigram. Furthermore, in good-risk patients with an undiagnosed pulmonary nodule, a completion lobectomy is performed when the lesion is a nonadvanced NSCLC. During the excision, the lung is deflated using a single lung ventilation technique in cases undergoing video-assisted thoracic surgery or a thoracotomy.

The end point of the present study was to determine the malignant status of each surgical margin, which was considered malignant positive when either a histologic or cytologic technique revealed a malignant positive status. A malignant negative conclusion required both the histologic and cytologic techniques to reveal malignant negative status. Maximum tumor diameter, margin-distance, tumor location, extent of stapling carried out, and performance of a thoracotomy (video-assisted thoracic surgery or other procedure) were used as variables.

Patient backgrounds
This study was conducted from September 1999 to September 2002. The ratio of contribution by the individual institutions was 172 regions by Toneyama National Hospital, 29 regions by National Kinki-Chuo Hospital for Chest Diseases, two regions by Osaka University, Graduate School of Medicine, and two regions by Habikino Hospital, and a total of 202 patients with 205 lesions were enrolled after providing informed consent to the study protocol. A flow chart of the patients is shown in Figure 1. Of the 205 excised lesions, 22 (9%) were preoperatively diagnosed as NSCLC and 183 (91%) were preoperatively undiagnosed lung nodules. After surgery, 118 lesions from 115 patients were confirmed to be NSCLC, which were included in the present study. Three of these patients had 2 lesions, of whom 2 had synchronous lesions, and 1 had a metachronous lesion. Seventy-seven of the NSCLC patients underwent a residual lobectomy for a preoperatively undiagnosed lesion that was diagnosed as NSCLC during surgery, and 41 lesions in 38 patients were resected using an excision technique alone. The reasons for not performing completion lobectomy were cardiopulmonary impairment in 33 patients with 35 lesions and age (greater than 80 years old) in 5 patients with six lesions. Of those who had lesions with a malignant positive margin, 37 patients could not undergo further proximal resection because of an anatomical difficulty.



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  		Fig 1. Flow chart of patients. (NSCLC = nonsmall cell lung cancer; UDLT = undiagnosed lung tumor.)

 
Surgery
All lesions were wedge-resected and three stapling methods were used. In the first method, the complete area of the surgical margin was stapled, which was classified as complete. In the second method, most of the surgical margin area was stapled and the remaining area was resected using a tool other than a stapler, which was classified as partial. In the third method, the whole area was resected using a tool other than a stapler, which was classified as not used. However, staplers were used predominantly, but only partially when the remaining proximal parenchyma of the lung was too thick to be stapled. A laser or an electrosurgical unit was used when a lesion was located deep inside the lung.

Tumor locations were divided into two regions according to the method of Lewis and colleagues [16]. Thus, lesions in the lingual, apex, and lung edge areas were defined as easily resectable, whereas those in the base of the lung, deep in a fissure, or on a large ovoid surface were defined as difficult to resect.

Cytopathological diagnosis of the surgical margin
Cytologic examinations of the surgical margins were carried out using the run-across method and were undertaken before the cross-section was studied, in order to prevent malignant cell contamination by the tumor. To extract the specimen, a glass slide was run across the whole of the stapled area at least three times until a sufficient amount of material was collected. The extracted sample was spread onto another glass slide and immediately fixed with ethanol spray. After the materials for cytologic examination were extracted, the wedge-resected specimen was cut and examined grossly. The distance from the tumor to the margin was measured using a cross-section of the lesion without removing the staples, which provided the maximum diameter of the tumor. The materials from the margin were stained with half-time Papanicolaou stain before being examined. A positive result was defined as at least three malignant cells or clustered malignant cells being observable on the glass slide. Afterward, the specimen was examined by pathologic means. Staples, if any, were removed for pathologic examination.

Statistical analysis
Statistical analyses were performed using a commercially available software package (Stat View 5.0 [Abacus Computer, Berkeley, CA]). Maximum tumor diameter, margin distance, tumor location, extent of stapling carried out, and performance of a thoracotomy were used as vari-ables. To compare maximum tumor diameter and margin distance in the malignant positive and malignant negative groups, a t test was used. To compare the prevalence of tumor location, the extent of stapling carried out, and the performance of a thoracotomy, a {chi}2 test and Fischer's exact test were used as appropriate. Univariate logistic regression analyses were carried out using all five variables. A multivariate logistic regression analysis was carried out using variables from the univariate analysis results that were statistically significant. Significance was considered when a p value was less than 0.05.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Characteristics of pulmonary malignant tumors that underwent excision
Prevalence rates for the five variables are shown in Table 1. The NSCLC subtype was adenocarcinoma in 104 lesions, squamous cell carcinoma in 12 lesions, and large cell carcinoma in two lesions. Prevalence rates of the histologic and cytologic diagnoses are shown in Table 2. Eighty-four of 118 surgical margins (71%) had matching histologic and cytologic diagnoses. At the time this article was written, there were 6 cases of margin relapse, 2 of which were both histologically and cytologically malignant positive, and 4 that were cytologically malignant positive only.


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  		Table 1. Characteristics of Excised Pulmonary Malignant Tumors

 

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  		Table 2. Comparison of Prevalence Between Histology and Cytology Results

 
Comparisons of variables between negative and positive groups
Statistically significant differences were observed between the negative and positive groups for maximum tumor diameter, margin distance, tumor location, and extent of stapling, but not for performance of a thoracotomy (Table 3).


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  		Table 3. Comparison Between Malignant Positive and Malignant Negative Groups

 
Logistic regression analyses
In univariate analyses, maximum tumor diameter, margin distance, tumor location, and extent of stapling were statistically significant among the five variables (Table 4). A multivariate analysis was then carried out using these four variables, and only maximum tumor diameter and margin distance were found to be independent factors (Table 5).


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  		Table 4. Univariate Analyses Using Logistic Regression Model

 

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  		Table 5. Multivariable Analyses Using Logistic Regression Model

 
Further analysis using maximum tumor diameter and margin distance
We conducted a further analysis using the two independent factors in order to identify the threshold distance. The ratio of margin distance to maximum tumor diameter in the negative group was 0.9 ± 0.6 (mean ± standard deviation) as compared with 0.3 ± 0.3 in the positive group (p < 0.0001). In every positive case, the sum of margin distance divided by maximum tumor diameter was less than 1 (Fig 2). Furthermore, there was no malignant surgical margin found among the seven lesions that had a margin distance greater than 2 cm, which is generally believed to be a safe margin distance [17].



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  		Fig 2. Margin distance from tumor compared with the maximum tumor diameter according to malignant status at surgical margin of excised tumor. The margin distance from the tumor as compared with the maximum tumor diameter was 0.9 ± 0.6 cm (mean ± standard deviation) in the negative group and 0.3 ± 0.3 cm (mean ± standard deviation) in the positive group (p < 0.0001). In every positive case, the sum of the margin distance from the tumor divided by the maximum tumor diameter was less than 1.

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
One of the most serious problems of a limited resection in cases of NSCLC is a high rate of surgical margin relapse [1–7], whereas the Lung Cancer Study Group has suggested a diminished survival rate among patients who undergo resection less than a lobectomy. Therefore, an appropriate technique must be applied to avoid such relapse. Postoperative radiation therapy can reduce the risk of local recurrence [9] and its role after wedge resection, which is currently being investigated in a prospective study [18]. Brachytherapy has also been attempted during operations [19] with preliminary results revealing no instances of significant radiation pneumonitis or local recurrence. Although these treatments may reduce the risk of margin relapse, an adequate margin distance remains the strongest defense.

There is no clear information regarding what constitutes an adequate margin distance when a wedge resection is performed. Allen and Parirolero [20] recommended a margin of 1 cm in cases with a malignant nodule, whereas it is commented that a margin of 1.5 cm in a deflated lung and 2 cm in an inflated one are generally acceptable in a textbook of thoracic surgery [17]. However, scant data have been reported regarding the size of margins obtained. As described in our previous study [14], a margin relapse can occur even if a wedge-resected NSCLC has a margin of more than 1 cm, or 1.5 cm in a deflated lung, as well as malignant negative histology findings. Furthermore, it has been found that margin relapse occurs only in cases of a cytologically malignant positive margin [12–15]. In addition, another disadvantage of wedge resection is blindness in relation to the segmental and interlobar lymph nodes.

Attaining a malignant negative surgical margin is very important to prevent margin relapse, and Lewis and colleagues reported [16] that both size and location of the tumor are directly related to the margin obtained. In the present study, a univariate analysis revealed a high number of lesions that were difficult to resect and a shorter margin distance in the positive group. In addition, maximum tumor diameter and type of stapling used had an influence on the malignant status of the surgical margin. Although the performance of a thoracotomy was not statistically significant, the average distance from the margin to the tumor in thoracotomy cases was smaller than that in video-assisted thoracic surgery cases. This was likely because of the selection bias in both thoracotomy and video-assisted thoracic surgery cases, as well as technical limitations. When a multivariate analysis was carried out, both margin distance and maximum tumor diameter were independent variables. Therefore, it is important to obtain as great a margin distance from the surgical margin to the tumor as possible regardless of tumor size.

The margin distance from the tumor can also restricted by anatomical issues. For example, removal of a tumor with a 1.0 or 1.5 cm margin that is located in a difficult region to resect may be complicated, as the margin distance obtained is relative to tumor size. If the removed tumor is 0.5 cm in size, then a 1.5 cm margin may be sufficient, whereas the same size margin with a tumor 3 cm in size would likely be insufficient. Therefore, analysis using the two independent variables to determine the ratio of the distance from the surgical margin to the tumor diameter is mandated.

The rate of malignant negative margin occurrence was 100% when a tumor was resected with a greater margin distance from the surgical margin to the tumor than the maximum tumor diameter. That is, the distance threshold of the malignant-safe margin was equal to the maximum tumor diameter. The run-across method can reveal the malignant status of a surgical margin [12, 14]; therefore, using this technique during surgery is strongly recommended. However, a margin distance of greater than maximum tumor diameter in a deflated lung may be a good measurement to insure a malignant-safe margin, if the run-across method cannot be utilized.

There were some limitations to this study. The number of high-risk patients was 41 (39%), whereas 77 (61%) had a normal lung. There may have been patho-anatomical differences between these two groups of patients, but an insufficient margin distance was permitted because a complete lobectomy for NSCLC was utilized in cases of nondiagnosed pulmonary nodules. Thus, the distance threshold for a malignant negative surgical margin was able to be determined.

In conclusion, a multicenter, prospective study revealed that when an NSCLC tumor was excised, malignant positive margins were not found when the margin distance was greater than the maximum tumor diameter. This amount of distance is warranted to prevent margin relapse in cases of NSCLC excision.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
We appreciate the cooperation of Satoru Yamamoto, MD, of the Division of Clinical Pathology at National Kinki-Chuo Hospital for Chest Diseases; cytopathologist, Taikichi Hashimoto at Toneyama National Hospital for cytologic diagnosis of the harvested materials; and the cooperation of the members of Thoracic Surgery Study Group of Osaka University: Masahito Ikeda, MD, at Otemae Hospital; Kiyohiko Fijiwara, MD, and Masayoshi Inoue, MD, at Habikino Hospital; Shin-Ichi Takeda, MD, Yoshitomo Okumura, MD, and Teruaki Asada at National Toneyama Hospital; and Hirohisa Hirabayashi, MD, at Osaka University Graduate School of Medicine.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

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