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Ann Thorac Surg 2010;89:877-883. doi:10.1016/j.athoracsur.2009.11.037
© 2010 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Superselective Segmentectomy for Deep and Small Pulmonary Nodules Under the Guidance of Three-Dimensional Reconstructed Computed Tomographic Angiography

Kembu Nakamoto, MD, PhDa,*, Ken-ichi Omori, MD, PhDb, Kenji Nezu, MD, PhDc, Lung Cancer Project Group of West-Seto Inland Sea, Japan

a Division of General Thoracic Surgery, Memorial Shunan Hospital, Kudamatsu City, Yamaguchi, Japan
b Division of General Thoracic Surgery, National Kure Medical Center, Hiroshima, Japan
c Department of Surgery, National Ehime Hospital, Tou-on city, Ehime, Japan

Accepted for publication November 12, 2009.

Abbreviations and Acronyms AAH = atypical adenomatous hyperplasia; actFEV1 = actual forced expiratory volume in one second after the operation; BAC = bronchioloalveolar carcinoma; CT = computed tomography; 3D-CT angio = 3-dimensional reconstructed CT angiography; DS = daughter segmentectomy; GGO = ground glass opacity; MDR-CT = multidetector-row CT; PrdFEV1 = preoperatively predicted forced expiratory volume in one second after the operation; SS = subsegmentectomy; SSS = superselective segmentectomy

* Address correspondence to Dr Nakamoto, Division of General Thoracic Surgery, Memorial Shunan Hospital, 1-10-1 Ikunoya minami, Kudamatsu city, Yamaguchi 744-0033, Japan (Email: nakamoto{at}hcsdojinkai.or.jp).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: Three-dimensional computed tomographic angiography (3D-CT angio) allows selective access to peripheral segments. Superselective segmentectomy (SSS) was applied to the surgical management of indeterminate small and deep pulmonary nodules.

Methods: Thirty patients with indeterminate pulmonary nodules less than 25 mm in diameter and located deeper than 20mm from the pleural surface were enrolled in this study between 2002 and 2009. All patients underwent exploratory thoracotomy. The SSS with a surgical margin from the nodule larger than the nodule diameter or 20 mm was directed toward the target pulmonary arteries by 3D-CT angio using a multidetector-row CT scanner. The SSS was evaluated for resected area, surgical margin, regional lymph nodes, morbidity, lung function, and survival rate.

Results: Three patients received SSS at the daughter segment, 23 patients that at the subsegment, and the remaining four underwent miscellaneous SSS without major complications. Twenty patients exhibited early lung cancer, one patient stage IIA lung cancer, and the remaining nine patients had metastatic or benign tumors. Five patients with primary cancer subsequently underwent standard lobectomy. The remaining 16 patients with early lung cancer did not undergo lobectomy because of their major comorbidities or refusal of a second thoracotomy. The surgical margins were free of disease in all patients. The actual and disease-free five-year survival rates were 100% for the lung cancer patients, excluding those who subsequently underwent lobectomy. The lung function after SSS was well preserved.

Conclusions: Superselective segmentectomy is an applicable optional strategy for the surgical management of indeterminate small and deep pulmonary nodules.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Indeterminate small pulmonary nodules often warrant excisional biopsy to detect early lung cancer [1, 2]. Some nodules are resected by excessive resection owing to their deep localizations [1, 3]. These nodules frequently consist of benign or metastatic tumors, even after careful selection [2, 4]. Additionally, the limited diagnostic accuracy of using frozen sections [5] sometimes necessitates a second thoracotomy for standard lobectomy after a confirmatory diagnosis using permanent sections. Some optional strategies are required to resolve these conflicts in the surgical management of indeterminate nodules. The increased interest in limited operation as the primary therapy for early lung cancer led thoracic surgeons to begin to selectively use sublobar resection in lieu of lobectomy [6]. Three-dimensional computed tomographic angiography (3D-CT angio) provides clear images of the intrapulmonary vascular branches [7]. It allows superselective access to more peripheral segments than conventional segmentectomy [8] as a tool for aiding anatomic pulmonary resection. These results suggested the feasibility of more peripheral anatomic resection against indeterminate small nodules. The purpose of this study is to investigate the clinical feasibility of superselective segmentectomy (SSS) for the surgical management of indeterminate small pulmonary nodules located deep in the lung parenchyma.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Our institutional review board approved this study and individual patient consent for SSS and participation in this study was obtained. Thirty patients with indeterminate pulmonary nodules measuring less than 25 mm in diameter were enrolled in this prospective study from January 2002 to May 2009. All patients underwent an excision biopsy by SSS for definitive diagnosis of the nodules with ground glass opacity (GGO) or solid density on CT scans [9]. The nodules were located in regions defined as difficult for wedge resection by Lewis and colleagues [10]. All nodules were also located at a depth greater than 20 mm, which is considered to be too far from the pleural surface [11] for detection on CT scans. Definitive diagnosis of GGO nodules was carried out using permanent sections and that of solid nodules was carried out using frozen or permanent sections. Patients without comorbid disease subsequently underwent standard lobectomy if frozen or permanent sections showed primary lung cancer. Patients with multiple nodules at 3 or less sites underwent SSS for the main nodule and wedge resection for the other nodules.

The target vascular branching patterns were evaluated preoperatively by 3D-CT angio. A multidetector-row CT scanner (MDR-CT) (Light Speed Plus, GE, Milwaukee, WI; Aquilion 64, Toshiba Medical, Tokyo, Japan) was used to obtain 3D-CT pulmonary arterial images. Helical CT data (beam pitch of 0.75 and 1.25 mm reconstruction intervals) concerning the pulmonary vasculature, with intravenous contrast medium infusion (Iopamiron 100 mL, 3.0 mL/second; Bayer Schering Pharma; Berlin, Germany) under a start delay of 18 seconds, were acquired from the main pulmonary artery to the target nodule in one 25-second or 8-second breath hold. Three dimensional angiographic images were reconstructed using Workstation software (Advantage Windows, ADW ver3.1, Medical Systems, Milwaukee, WI; Ziostation, NG1 ver1.17q, Toshiba Medical, Tokyo, Japan). The planar operative procedure was simulated to maintain surgical margins from the nodule that were larger than the nodule itself or 20 mm, as suggested by Sawabata and colleagues [12] using 3D-CT images.

The numbering and symbols used to denote pulmonary segments and peripheral bronchovascular branches followed the method of Yamashita‘s Roentgenologic Anatomy of the Lung [13]. Consequently, the anterior and the posterior segments of the right upper lobe are termed S3 and S2, respectively, and the anterior and the apical posterior segments of the left upper lobe are S3 and S1+2, respectively. There is no precise international rule for the numbering of daughter branches, so the consensus reached by the Japanese Committee on the Nomenclature for Bronchial Branching was adopted in this study [14] (Fig 1[A]). Subsegmentectomy (SS) is defined as pulmonary segmentectomy at the subsegmental (third order) arterial and bronchial branches. Daughter segmentectomy (DS) is defined as segmentectomy at the next distal order (fourth order) branches.


Figure 1
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  		Fig 1. (A) Peripheral segments reproduced from the consensus arrangement produced by the Japanese Committee on the Nomenclature for Bronchial Branching (solid line = intersegment plane; fine solid line = inter-subsegment plane; broken line = interdaughter segment plane; S1 to S10 = segments; a, b, c = subsegments; i, ii = daughter segments). The right S7 is deleted. (B) Nodule locations. (Open circle, open square, and triangle = ground glass opacity nodules less than 10 mm, 10 to 20 mm, and 20 mm~, respectively. Closed circle and square = solid nodules less than 10 mm and 10 to 20 mm, respectively.)

 
All patients underwent posterolateral thoracotomy under double lumen endotracheal intubation, and the feasibility of wedge resection or core needle biopsy [15] at the thoracotomy was initially assessed. The operative procedure was virtually the same as that for a formal segmentectomy, except for the greater peripheral exposure of the arterial and bronchial branches. The mediastinal or interlobar veins of the right upper lobe or the mediastinal veins of the superior segment of the left upper lobe were initially taped and retracted to expose the peripheral arteries of the right upper lobe or the left anterior segment. The intersegment plane was separated by blunt dissection by traction of the divided target bronchi and arteries, and some parts were divided with electrosurgical units or staplers. If bullous disease blurs the distinction of the segment boundary, the resection range could be extended. Staplers, which are convenient for conventional segmentectomy [16], were not used to divide the intersegment plane to preserve intersegment veins and to obtain accurate surgical margins as simulated on 3D-CT whenever possible. Principally, the raw segmental surface was neither closed nor covered with the adjacent pleural surface. The dissected raw parenchyma surface was sealed with minimal use of fibrin glue after closing any active air leaks with 4-0 monofilament sutures. Regional lymph nodes from no. 11 to no. 14 were dissected upon detection during the procedure. The surgical margins for residual cancer were examined in accordance with Sawabata and colleagues [12].

The effect of SSS on postoperative lung function was evaluated using the actual forced expiratory volume in 1 second (actFEV1) compared with the preoperatively predicted FEV1.0 (prdFEV1) calculated by the formula of Nakahara and colleagues [17]: prd FEV1 = {1 – (number of resected subsegments)/(42 or total number of subsegments)} x preoperative FEV1.0 (L). Daughter segments were assumed to have half the volume of the subsegment in this study.

The survival rates by Kaplan-Meier statistics and linear regression between prdFEV1 and actFEV1 were examined with commercially available software (Stat View ver. 5.0, Abacus Computer, Berkeley, CA). Data were expressed as mean ± standard error.


   Results
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 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Eighteen of the thirty patients were female. The patients' ages ranged from 40 years to 84 years (68.5 ± 7.9 years). Twelve patients exhibited nodules with GGO and the remaining 18 exhibited solid density on CT scans. Nodule size ranged from 5 to 25 mm (12.8 ± 5.4 mm) in diameter as measured on CT scans. Sixteen patients had nodules in the right lung and fourteen in the left lung (Fig 1[B]). Twenty-one patients showed primary lung cancer. Six patients showed metastatic lung tumors, and the remaining three showed benign nodules (Fig 2). Eleven of the 12 GGO patients exhibited primary lung cancer of adenocarcinoma or bronchioloalveolar carcinoma (BAC) with Noguchi and colleagues' type A–C [18], and the remaining patient exhibited atypical adenomatous hyperplasia (AAH). Frozen sections of 5 patients led to a provisional diagnosis of either BAC or AAH, and either adenocarcinoma or metastatic tumor from breast cancer. Among 21 lung cancer patients, 20 had stage IA and the other patient with a solid nodule had stage IIA lung cancer. All dissected lymph nodes including intrapulmonary nodes were negative, except one that had stage IIA lung cancer for positive interlobar lymph nodes. Five patients subsequently underwent standard lobectomy due to primary lung cancer with or without positive nodes identified in frozen or permanent sections. Nine lung cancer patients did not undergo formal lobectomy because of conditions including chronic respiratory failure, previous pulmonary resection on the contralateral side, dialysis-dependent renal failure, chronic heart failure, or being older than 80 years. Seven patients with early lung cancer of GGO refused subsequent operations after receiving pathologic reports and the results of limited operations for early lung cancer. All these 16 patients who did not undergo standard lobectomy had stage IA lung cancer. Surgical margins were free of residual disease in all patients.


Figure 2
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  		Fig 2. Diagram of diagnosis and treatment process. (AAH = atypical adenomatous hyperplasia; Ad = adenocarcinoma; BAC = bronchioloalveolar carcinoma; compromised = compromised condition with major comorbidities; CT = computed tomography; GGO = ground glass opacity; LC = lung cancer; meta = metastatic tumor; N0,1 = lymph node status; SSS = superselective segmentectomy; () = number of patients.)

 
Daughter segmentectomy was performed on three patients, SS on 23, a combination of DS and SS on two, and a combination of SS with conventional segmentectomy on two (Table 1). One of the three DS patients exhibited a tiny GGO nodule at the intersegmental area. The patient underwent a combination of DSs on different contiguous segments. The 3D-CT angio detected the target pulmonary arteries branching from the same parent branch originating in the truncus superior (Fig 3[A] [B]). The other two DSs consisted of a single DS for small GGO nodules. All target nodules that could not be detected by palpation in these three patients were correctly accessed and resected with sufficient surgical margins. Eight of the 23 SS patients exhibiting small nodules in an intersegment area underwent a combination of SS on contiguous segments. The remaining 15 of the 23 SS patients had single or bi-subsegments resected in a single segment. The SSSs related to the anterior segments in the upper lobes were the most frequently performed procedures. Access to the target arteries in the upper lobes required mediastinal and (or) interlobar approaches (Fig 3[C],[D]). The SSSs in the lower lobes only required an interlobar approach. However, access to the posterobasal segment required sacrifice of bi-subsegments for anatomic reasons.


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  		Table 1 Operative Procedures of Superselective Segmentectomy
 

Figure 3
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  		Fig 3. (A) A tiny pulmonary nodule that showed ground glass opacity on computed tomography (CT). (B) A three-dimensional (3D)-CT angiography of the topographic relationship between the nodule and the target arteries in a single patient who underwent a combination daughter segmentectomy of S1aii and S2ai. (C) A ground glass opacity nodule on CT. (D) A 3D-CT angiography of the topographic relationship between the nodule and the target arteries. The target arteries A3b and A3c shared a common parent artery with A3a (recurrent type), and the patient underwent bi-subsegmentectomy of S3b and S3c. This branching pattern allowed mediastinal access for the surgical procedure.

 
There were no major postoperative complications. The mean operating time for SSS was 228 ± 63 minutes, including diagnostic time for frozen sections. Mean blood loss during the operation was 191 ± 156 g. Eighteen patients (excluding patients whose treatment had been switched to radical resection) exhibited no air leakage at the end of the operation. Seven patients exhibited air leakage for a period ranging from overnight to four days.

Twenty-two patients (excluding those switched to a lobectomy and those who underwent SSS with wedge resection for multiple nodules) were followed up with respect to their pulmonary function for three to six months after SSS. The actFEV1 correlated well with prdFEV1 as follows (Fig 4):


Formula

Postoperative lung function in SSS was well preserved, as preoperatively predicted.


Figure 4
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  		Fig 4. Postoperative lung function. Actual forced expiratory volume in one second after superselective segmentectomy (actFEV1) was well preserved as predicted before the operation (prdFEV1). (Solid line = actFEV1(L) = 0.925 x prdFEV1(L) –0.015 R2 = 0.924, p < 0.0001; broken line represents actFEV1 = prdFEV1.)

 
ActFEV1 was about 7.5% lower than prdFEV1, and this slight reduction might have been caused by the thoracotomy.

All patients in this study were followed up for an average period of 45.5 ± 20.9 months. Two patients who had primary lung cancer and metastatic tumor died at 44 and 16 months, respectively. A lung cancer patient who underwent conversion lobectomy died of malignant mesothelioma on the contralateral side. A patient with metastatic tumor died of her primary disease. There was no disease relapse or locoregional recurrence among the patients with lung cancer. The overall and disease-free five-year survival rates for the lung cancer patients were 93.3% and 100%, respectively. The rates for the lung cancer patients excluding those who underwent a subsequent lobectomy were both 100%.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The concept of an anatomic resection smaller than conventional segmentectomy [8] has not been applied to general thoracic surgery because of the substantial variation in the peripheral bronchovascular branching patterns within the lung parenchyma [13], and also the lack of apparent advantages over a segmentectomy or a wedge resection. Recent papers about anatomic segmentectomy for the management of small tumors have led to a resurgence of interest in less invasive anatomic resection [6, 16, 19]. We applied SSS as a minimal anatomic resection in the diagnostic procedure. The most complex factor involved in the SSS procedure is the high variability of arterial branching patterns. Improvements in helical CT scans have provided fine 3D images that illustrate the topographic relationship between the target nodule and the surrounding vessels [7], and this has allowed access to more peripheral vascular branches and their accurate detection during the procedure. The 3D-CT angio by MDR-CT provides a means of assessing the arterial branching pattern down to fifth-order branches [20]. In this study, 3D-CT angio allowed evaluation of the daughter segment arteries. Preoperative vascular evaluation by 3D-CT angio provided an accurate simulation for planar operative procedures, satisfying the requirement for a sufficient surgical margin greater than the nodule size or 20 mm [12, 16]. The daughter segment is the minimum unit for an anatomic resection that satisfies this criterion. Access to the target arteries depended on their branching patterns, especially in both upper lobes. This complicated procedure for exposing peripheral arteries and bronchi required a surgical duration comparable with that of conventional lobectomy or segmentectomy. The SSS was not applied to the middle lobe in this study. However, this surgical procedure is applicable to all segments, including the anterior, posterior, or apical-posterior segments of the upper lobes and the posterolateral basal segments of the lower lobes.

To ensure a high probability of detecting very small pulmonary nodules on helical CT scans [21, 22], wedge resection under video-assisted thoracoscopic surgery or exploratory thoracotomy is frequently required to confirm the diagnosis [1, 2] after careful observation by CT scans [9], or, occasionally, positron emission tomography [4, 23]. These nodules are sometimes located deep within the lung parenchyma where wedge resection is restricted and excessive resection by lobectomy or single, bisegmentectomy, or trisegmentectomy is required [1, 3], while indeterminate nodules frequently contain benign nodules [1, 2, 4]. In addition, the limitations of using frozen sections for differential diagnosis between lung cancer and a benign tumor, especially between BAC and AAH [5], may require a second thoracotomy for standard lobectomy after confirmatory diagnosis of lung cancer using permanent sections. There is an increased interest in limited resection for stage IA lung cancer [23–25]. In particular, small BACs with GGO are considered in situ carcinomas [18], and in some reports limited resection is suggested for these nodules [26, 27]. The SSS was optionally applied to resolve these conflicts of surgical management for indeterminate small nodules. Deep wedge resection with staplers as an alternative to lobectomy or segmentectomy for deep nodules has the risk of providing an inadequate seal of densely packed parenchyma [28], resulting in massive hemorrhages or air leakage and, occasionally, lack of pulmonary reexpansion [29]. Wedge resections for these deep and small nodules also carry the risk of generating residual cancer at the surgical margin [10], or of missing the target nodules [11]. Nodules with GGO, such as BAC, were especially difficult to locate even with manual palpation. Furthermore, wedge resection carries the risk of generating malignant positive lymph nodes at the proximal region [6]. The SSS provided greater peripheral lymph node sampling, in addition to hilar and mediastinal lymph nodes. In our series, a lung cancer patient with a solid nodule that was found to have metastasized to an interlobar node was switched to a formal lobectomy. None of the lung cancer patients with GGO had positive peripheral lymph nodes. These findings suggest that the prevalence of lymph node metastasis is minimal in small nodules measuring less than 20 mm in diameter, especially in those with GGO [6, 18, 24]. Investigations of sentinel lymph nodes, for example, may allow better understanding of peripheral lymphatic tumor drainage [30] and facilitate the determination of lymph node status in sublobar anatomic resection. However, our procedure achieved accurate analysis of lymph node status resulting in no locoregional recurrence like that in conventional segmentectomy [31]. No patients had positive surgical margins greater than the nodule size or 20 mm. Our results support recent findings about the application criterion of sublobar resections for the management of stage IA small lung cancer: nodules measuring less than 20 mm in diameter with a surgical margin greater than the nodule size or 20 mm [12, 16]. Lung cancer frequently involves intersegmental areas and requires excessive resection [32]. The typical limited resections performed against this type of tumor are a nonanatomic wedge resection, combination segmentectomy [8], or segmentectomy with partial resection of the adjacent segments [33]. The SSS for a very small nodule, by combination DS or SS, results in more extensive removal of tumor-related contiguous segments than partial resection with or without segmentectomy. This procedure also resulted in no local relapse during the follow-up period. The lung tissue loss caused by combined SS is comparable with that caused by a single segmentectomy, but normal areas of the target segment are preserved. Postoperative lung function after SSS was well preserved as preoperatively predicted. Superselective segmentectomy might be applicable as an optional strategy for the surgical management of indeterminate small nodules.

Three-dimensional reconstructed CT angiography allowed superselective access to greater peripheral segments and enabled accurate anatomic resections of deep small pulmonary nodules in both upper and lower lobes with minimal volume loss. The SSS technique can be applied as part of surgical strategies for treating indeterminate small pulmonary nodules.


   References
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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