Gen Thorac Cardiovasc Surg DOI 10.1007/s11748-014-0409-7
CURRENT TOPICS REVIEW ARTICLE
Anatomical thoracoscopic segmentectomy for lung cancer Yoichi Ohtaki • Kimihiro Shimizu
Received: 31 March 2014 Ó The Japanese Association for Thoracic Surgery 2014
Abstract Minimally invasive surgery for lung cancer has seen considerable progress. A segmentectomy is less invasive than a lobectomy as it preserves lung parenchyma. The preservation of pulmonary function can reduce complications. The combination of a thoracoscopic approach with a segmentectomy should be less invasive, and retrospective studies have shown that the thoracoscopic approach is safe and feasible due to the lower postoperative mortality and complication rates as compared to an open thoracotomy. The validity of a segmentectomy for groundglass-opacity-type lung cancer has been demonstrated, and it has also been evaluated for small, predominantly solid, lung cancers. Two prospective studies of segmentectomy versus lobectomy for B2-cm non-small-cell lung cancer are now underway (CALGB 140503 and JCOG0802/ WJTOG4607L) and should clarify the role of segmentectomy. Regarding thoracoscopic segmentectomy, few retrospective studies have reported the oncological outcome for lung cancer and there is inadequate evidence regarding the long-term oncological outcome, although the perioperative complication rate and duration of hospital stay seem to be non-inferior to those of an open approach. For preoperative simulation, three-dimensional multidetector computed tomography (3D-CT) is essential for performing an atypical thoracoscopic segmentectomy safely. Preoperative 3D-CT angiography and bronchography (3D-CTAB) enable accurate identification of the venous branches in the
This review was submitted at the invitation of the editorial committee. Y. Ohtaki K. Shimizu (&) Department of Thoracic and Visceral Organ Surgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan e-mail: [email protected]
affected segment and the intersegmental vein. This review describes the surgical and oncological outcomes, utility of 3D-CTAB, and surgical techniques and procedure used for a thoracoscopic segmentectomy. Keywords Lung cancer Thoracoscopic Segmentectomy Video-assisted thoracic surgery (VATS) Three-dimensional computed tomography (3D-CT)
Introduction Minimally invasive surgery for the treatment of thoracic malignancies has been evolving since the 1990s. There are three methods of minimally invasive lung cancer surgery: thoracoscopic or robotic surgery with limited access to the thoracic cavity and minimal chest wall damage using a thoracoscope without a mechanical retractor and without rib spreading; segmentectomy, wedge resection, or sleeve resection with reduced resection of the pulmonary parenchyma; and selective lymph node dissection [1]. Currently, lobectomy and systemic lymph node dissection are considered the standard surgical procedure for patients with completely resectable clinical stage I nonsmall-cell lung cancer (NSCLC) [2]. Segmentectomy is used mainly for patients with metastatic lung tumors or primary lung cancer and reduced pulmonary function, or older patients. However, high-resolution computed tomography (HR-CT) allows us to detect small lung cancers. As a result, non-solid tumors appearing as groundglass opacities [3], suggestive of noninvasive lung cancer with a good prognosis, are being detected increasingly commonly. The validity of a segmentectomy for GGO or GGO-type lung cancer has been demonstrated [4–7], and it has also been evaluated as a treatment for small
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predominantly solid lung cancers. Correspondingly, the safety of thoracoscopic surgery or video-assisted thoracic surgery (VATS) has been established for segmentectomy for lung cancer. In Japan, segmentectomies for primary malignant pulmonary tumor were performed in 3176 (9.6 %) of the 33,112 lung cancer cases in 2010 and more than two-thirds of the segmentectomies were performed by thoracoscopic surgery [8]. In conjunction with these circumstances, this review describes the surgical and oncological outcomes, and surgical techniques and procedure, including the use of threedimensional computed tomography (3D-CT) angiography and bronchography (3D-CTAB) for thoracoscopic segmentectomy.
Benefits of segmentectomy over lobectomy for lung cancer In 1995, a prospective multi-institutional randomized trial conducted by the Lung Cancer Study Group (LCSG) showed that limited resection, including wedge resection and segmentectomy, was associated with a poorer overall survival and higher regional recurrence rate as compared with lobectomy [9]. Another study confirmed the increased survival risk of segmentectomy over lobectomy, especially for tumors larger than 3 cm [10]. Since then, anatomical segmentectomies have been reserved for patients with poor cardiopulmonary function or the elderly. However, the prospective LCSG study included many non-anatomical wedge resection cases, which could have led to the worse survival [11, 12]. Some reports have demonstrated that the oncological outcome of segmentectomy is not inferior to that of lobectomy, considering tumor diameter [13–24]. However, Whitson et al. found that lobectomy conferred a significant survival advantage compared with segmentectomy regardless of tumor size in a population-based analysis [25]. In a meta-analysis comparing segmentectomy with lobectomy for early stage NSCLC, Bao et al. reported that although lobectomy was superior to segmentectomy for Stage I or IA tumors, segmentectomy was equivalent to lobectomy for tumors B2 cm [26]. Two prospective studies of segmentectomy versus lobectomy for B2 cm NSCLC are now underway—the phase III randomized trials CALGB 140503 and JCOG0802/WJTOG4607L—and should clarify the role and feasibility of segmentectomy [27]. Furthermore, a prospective single-arm phase III trial for clinical T1N0 (B3 cm) lung cancer dominant with GGO is also now under survey (JCOG 1211), and is expected to clarify the feasibility of segmentectomy for GGO predominant lung cancer. One of the greatest benefits of segmentectomy compared with lobectomy is the improved postoperative pulmonary
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function due to the preservation of lung parenchyma [28, 29]. If curability and the local recurrence rate are secured, the preservation of pulmonary function will be a great advantage, especially for the elderly. In 2009, Kilic et al. reported that elderly patients who underwent segmentectomy had fewer major complications than those undergoing lobectomy (11.5 vs. 25.5 %) [13]. Although the difference was not significant (p = 0.24), the operative mortality was 1.3 % for the segmentectomy group and 4.7 % for the lobectomy group. The disparity in the complication and mortality rates between the groups might be explained by the fact that the majority of patients in both groups were operated on using an open approach. Since the surgical technique of thoracoscopic segmentectomy is more complex than thoracoscopic lobectomy [30], the complication rates and lengths of hospital stay were similar in both the thoracoscopic segmentectomy and thoracoscopic lobectomy groups [14, 31–33].
Advantage of a thoracoscopic segmentectomy over an open segmentectomy Consequently, segmentectomy has been shown to be less invasive than lobectomy, and the combination of a thoracoscopic approach with segmentectomy should be less invasive. Thoracoscopic or VATS segmentectomies have been described in the last 10 years [14, 21, 31, 32, 34–46]. Table 1 summarizes the patients’ characteristics and operative variables. In this review, thoracoscopic or VATS surgery includes both total thoracoscopic surgery and hybrid VATS surgery. A thoracoscopic segmentectomy was initially performed for relatively simple procedures, such as the left upper division, lingular division, and superior (S6) or basilar segment of the lower lobes [14, 34, 37], which are typical segmentectomies in Table 1. In a retrospective study comparing thoracoscopic surgery with an open approach, Atkins et al. showed that a thoracoscopic approach reduced the length of hospital stay [37]. Shiraishi et al. also found that patients undergoing a thoracoscopic segmentectomy had a significantly shorter postoperative hospital stay than those with an open thoracotomy, despite the significantly longer operating time [35]. Schuchert et al. reported that a VATS segmentectomy was associated with a decreased length of stay (5 vs. 7 days, p \ 0.001) and fewer pulmonary complications (15.4 vs. 29.8 %, p = 0.012) compared with an open segmentectomy [39]. Although these were retrospective studies, all of them showed that a thoracoscopic approach was safe and feasible due to the lower postoperative mortality and complication rates as compared to those of open thoracotomy. Consequently, a thoracoscopic approach might require a longer operation duration, but patients
2011
2011
2011
2012
Gossot [43]c
Yamashia [44]
Oizumi [54]c
Okada [21]
153
424
TS
OS
13 31
TS
90
73
102
52
38
OS
TS
TS
TS
TS
TS
50
26
OS
TS
15
43
30
41
31
TS
TS
TS
TS
TS
121
OS
29
104
OS
TS
48
52
TS
TS
34 25
TS
No. of patients
OS
Approach
75
76
72
70
69
72
67
66
72
57
64
65
62
69
63
65
70
70
59
62
65
72
69
Age (mean)
NA
NA
NA
NA
46
100
50
37
55
74
42
33
100
40
78
100
65
79
90
94
52
NA
NA
Typical (%)
a
NA
NA
NA
NA
54
0
50
63
45
26
58
67
0
60
22
0
35
21
10
6
48
NA
NA
Atypical (%)
b
Type of segmentectomy
§
c
b
a
NA
NA
167
191
257 ± 91
NA
129
216
NA
188 ± 54
140 ± 38
145 ± 55
NA
216
220
NA
143
136
130 ± 65
136 ± 45
155
204 ± 69
240 ± 72
Operating time (min)
NA
0.212
–
–
–
–
–
–
0.70
–
–
–
–
0.42
0.68
–
0.05
p value
NA
NA
3.2
2.8
4.8 ± 3.4
NA
1
NA
NA
3.3 ± 1.9
5.2 ± 3.0
2.8 ± 1.3
NA
1
3±2
2
NA
NA
3.7 ± 1
3.5 ± 4
3
6.1 ± 4.9
4.5 ± 3.2
Chest tube duration (days)
NA
0.487
–
–
–
–
–
–
0.001
–
–
–
–
NA
0.7
–
NS
p value
NA
NA
12.7
8.5
12.2 ± 8.2
3.8 ± 3.3
NA
NA
NA
5.6 ± 2.4
8.3 ± 6.1
3.5 ± 1.4
NA
NA
NA
4
7
5
6.8 ± 6
4.3 ± 4
NA
16.7 ± 7.7
12.7 ± 3.6
Length of stay (days)
Atypical includes all other types of segmentectomy
Comparison of the percentage of extended length of stay
Includes metastatic lung tumor and benign tumor cases
0.03
0.020
0.01
\0.05§
–
–
–
–
–
–
–
–
–
–
\0.001
–
0.01
p value
Typical includes segmentectomy of the left upper division (S1 ? S2 ? S3), lingular division (S4 ? S5), and superior segment (S6) or basilar segment of lower lobe segmentectomy
TS thoracoscopic segmentectomy, OS open segmentectomy, NA not available, NS not significant
2014
2010
Leshnower [41]
Smith [48]
2010
Sugi [32]
2013
2009
Oizumi [40]c
Tarumi [64]c
2009
Watanabe [38]
2012
2009
Shapiro [14]
2012
2009
Schuchert [39]
Soukiasian [17]
2007
Yamashita [31]
2007
Okada [46]
2004
Shiraishi [35]
Atkins [37]c
Year
Author
Table 1 Summary of thoracoscopic segmentectomy compared with open segmentectomy in the literature
39.2
26.1
16.1
15.4
19
37
9.8
6
NA
10.2
NA
NA
NA
7
10
26
33.9
26.0
34.5
31.3
13.5
20
11.7
Complications (%)
0.24
0.81
0.999
\0.05
–
–
–
–
–
–
NA
–
–
–
–
–
NS
p value
\7.0
3.1
0
0
0
NA
0
0
0
NA
2
0
0
NA
0
0
1.7
0
6.9
0
NA
0
0
Mortality (%)
NS
NS
–
–
–
–
–
–
0.27
–
–
–
–
0.50
0.14
–
NS
p value
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might have less wound pain than would be the case using an open thoracotomy approach. Regarding operative complications, the thoracoscopic segmentectomy group had lower rates of pulmonary complications and infection [39]. A segmentectomy is a complex procedure because it requires dissection of the intersegmental plane and peripheral branch of the segmental artery or vein. With a thoracoscopic approach, the procedure must be performed despite the limited view of the surgical field [33]. Yang and D’Amico indicated that surgeon’s experience should be added as a factor in future analyses [47], because the outcome might be affected by the surgeon’s skill. From an oncological perspective, few retrospective studies have compared the outcome of thoracoscopic segmentectomy versus thoracotomy segmentectomy [37, 39, 48]. Atkins et al. reported that the VATS segmentectomy group had an improved overall survival compared with the open thoracotomy group [37]. However, both groups included pulmonary metastases and benign tumors, and there was a disparity in tumor size. Using propensity score methods, Smith et al. reported that the overall and lung cancer-specific survival was similar between the two groups in Stage I lung cancer patients older than 65 years [48]. Schuchert et al. found no significant differences in local and systemic recurrence and survival between patients undergoing VATS and open segmentectomy for stage I NSCLC [39]. Therefore, thoracoscopic segmentectomy had an inadequate benefit in terms of the long-term oncological outcome. However, the perioperative complications and duration of hospital stay were not inferior to those of an open approach. Comparing the outcome according to the surgical approach used is difficult because of differences in the technique among institutions. Therefore, the surgical approaches should be evaluated in largescale multi-institution studies in combination with the mode or extent of resection.
Technical considerations for segmentectomy and the utility of three-dimensional computed tomography angiography and bronchography With improvements in surgical techniques, the resection of segments or subsegments other than those described above as typical segmentectomies has been reported; these are listed as atypical segmentectomies in Table 1 [13, 28, 31, 35, 38–41, 43, 44, 49–54]. Oizumi et al. classified thoracoscopic segmentectomy into three categories according to the degree of procedural difficulty, classifying segments that involve the dissection of multiple surfaces at acute angles, or contain a bronchial pulmonary artery deep within as ‘‘difficult’’, such as S7 (medial-basal segment), S9
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(lateral-basal segment), and S10 (posterior-basal segment) [54]. Preoperative simulation using three-dimensional multidetector computed tomography (3D-CT) enables safe completion of a thoracoscopic segmentectomy [43, 49, 54– 60]. Previously, we described methods of identifying pulmonary vessel branches and segmental bronchi using 3DCT angiography and bronchography (3D-CTAB), and its benefits for segmentectomy [55]. Preoperative 3D-CTAB enabled us to identify the venous branches to the affected segment and intersegmental vein accurately, and to measure and plan the resection lines with an adequate surgical margin (Fig. 1). Figure 2 shows the 3D-CTAB image and operative findings of a segmentectomy case. The intrapulmonary anatomy, including the pulmonary artery, vein, and bronchus, varies greatly among patients. Consequently, the segmentectomy also varies because of the anatomical variation. Therefore, preoperative 3D-CTAB is essential for confirming the anomalous anatomy before a thoracoscopic segmentectomy [57]. Several procedures for recognizing the segmental plane have been reported. One technique for demarcating the segmental plane is to reinflate the ipsilateral lung temporarily after segmental bronchial ligation. Another is the selective jet ventilation method, which involves bronchoscopy into the involved segmental bronchus, as reported by Okada et al. [46]. We use this method because of its simplicity and safety. Kamiyoshihara et al. reported a method of inflating the involved segment using a butterfly needle [61]. Recently, Misaki et al. reported a method of identifying the segmental fissure using infrared thoracoscopy with indocyanine green (ICG) injection into a peripheral vein [62, 63], and confirmed its usefulness [64]. Oh et al. also reported a method using ICG injection into the involved segmental bronchus [65]. Each method has its advantages and disadvantages. For lung parenchymal dissection, several methods have been discussed, such as linear stapler and energy devices [46, 66, 67]. Electrocautery can be used to expand the residual lung parenchyma maximally and to obtain an accurate surgical margin [55]. A linear stapler is a comparatively simple method, and has been proposed to prevent prolonged air leakage, especially for emphysematous lung. After segmental resection, fibrin sealant and absorbable mesh for the resection line are useful for preventing prolonged postoperative air leakage [46, 68]. The most important aspect of a segmentectomy for lung cancer is securing a sufficient surgical margin. In cases of malignancy, the required surgical margin is greater than the tumor diameter or at least 2 cm of healthy lung tissue [46]. Furthermore, an HR-CT study reported that *30 % of c-T1aN0M0 NSCLC extends beyond one segment [69]. Therefore, segmentectomy of a single segment, which is
Gen Thorac Cardiovasc Surg Fig. 1 Three-dimensional multidetector computed tomography angiography and bronchography (3D-CTAB) images of the right a and left b lungs showing the pulmonary arteries (red) and veins (blue), and bronchi (yellow). The 3DCTAB image can be rotated as required
usually performed along the segmental vein with the aid of an inflation–deflation line, does not always provide an adequate surgical margin. Two methods can be used to obtain a sufficient surgical margin. One is used when the tumor is relatively close to the cutting line of the segmentectomy; the tumor is grasped within a ring-shaped forceps 3–5 cm in diameter and then the lung tissue is cut away from the forceps [70]. When the cutting line is beyond the intersegmental plane, a stapler is required to resect part of the neighboring segment. Alternatively, when preservation of the margin in a single-segment resection is difficult, an extended segmentectomy (a standard segmentectomy combined with resection of an adjacent segment or subsegment) is planned preoperatively using 3DCT and 2D-CT images [55]. The former method is technically easy, although it is difficult when the tumor cannot
be palpated or there is no access port for VATS beyond 3 cm. Therefore, we usually use the latter method for these situations.
New aspects of segmentectomy A novel technique to reduce the invasiveness of thoracoscopic segmentectomy is the single-port approach [71]. Gonzalez-Rivas et al. performed a single-port videoassisted thoracoscopic segmentectomy of the superior segment of the right lower lobe [72]. However, intensive training is necessary to perform single-port surgery and the size of the excised segment can be limited. A non-intubated thoracoscopic segmentectomy is another less-invasive method [72]. Hung et al. reported cases without intubation
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A
V1+2a+b
A3 B3 V3a+V1+2d
Furthermore, most of the reports reviewed were retrospective studies. The outcomes of two ongoing randomized controlled studies for B2 cm NSCLC (CALGB 140503 and JCOG0802/WJOG4607L) and one prospective single-arm trial for clinical T1N0 (B3 cm) lung cancer dominant with GGO (JCOG 1211) are expected in the near future. Conflict of interest All of the authors participated in this study and agreed on the content of this paper. None of them has any financial or other relationship that could lead to a conflict of interest.
V3c+V1+2c V3b
References
V4+5
B
V1+2a+b
A3 B3 V3a+V1+2d
V3c+V1+2c V3b
V4+5 Fig. 2 Left S1?2c ? S3a segmentectomy. a 3D-CTAB image at the hilum of the left upper lobe b Operative view of the patient. The hilum of the left upper lobe is exposed from the ventral to dorsal side to expose the superior pulmonary vein and arteries from the left main to the proximal site of the inter-lobar artery
using a combination of thoracic epidural anesthesia, intrathoracic vagal blockade, and target-controlled sedation [72]. Although the maneuver is complicated and requires a greater level of intraoperative attention, it might be useful in patients who are at high risk for general anesthesia. A robotic approach is an alternative procedure for segmentectomy [73]. However, robotic surgery will take a number of years to become widespread for reasons of cost and limited availability [74].
Limitations and future study This review included two types of thoracoscopic surgery: total thoracoscopic segmentectomy and hybrid VATS segmentectomy. Since they are very different approaches technically, it would be better to compare the outcome and operative data, although these would be influenced by the surgeon’s technique and the segment resected.
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32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47. 48.
classification of non-small cell lung cancer: a single center experience. Eur J Cardiothorac Surg. 2012;42:83–8. Sugi K, Kobayashi S, Sudou M, Sakano H, Matsuda E, Okabe K. Long-term prognosis of video-assisted limited surgery for early lung cancer. Eur J Cardiothorac Surg. 2010;37:456–60. Fournel L, Zaimi R, Grigoroiu M, Stern JB, Gossot D. Totally thoracoscopic major pulmonary resections: an analysis of perioperative complications. Ann Thorac Surg. 2014;97:419–24. Houck WV, Fuller CB, McKenna RJ Jr. Video-assisted thoracic surgery upper lobe trisegmentectomy for early-stage left apical lung cancer. Ann Thorac Surg. 2004;78:1858–60. Shiraishi T, Shirakusa T, Iwasaki A, Hiratsuka M, Yamamoto S, Kawahara K. Video-assisted thoracoscopic surgery (VATS) segmentectomy for small peripheral lung cancer tumors: intermediate results. Surg Endosc. 2004;18:1657–62. Iwasaki A, Shirakusa T, Shiraishi T, Yamamoto S. Results of video-assisted thoracic surgery for stage I/II non-small cell lung cancer. Eur J Cardiothorac Surg. 2004;26:158–64. Atkins BZ, Harpole DH Jr, Mangum JH, Toloza EM, D’Amico TA, Burfeind WR Jr. Pulmonary segmentectomy by thoracotomy or thoracoscopy: reduced hospital length of stay with a minimally-invasive approach. Ann Thorac Surg. 2007;84:1107–12 (discussion 12–3). Watanabe A, Ohori S, Nakashima S, Mawatari T, Inoue N, Kurimoto Y, et al. Feasibility of video-assisted thoracoscopic surgery segmentectomy for selected peripheral lung carcinomas. Eur J Cardiothorac Surg. 2009;35:775–80 (discussion 80). Schuchert MJ, Pettiford BL, Pennathur A, Abbas G, Awais O, Close J, et al. Anatomic segmentectomy for stage I non-small-cell lung cancer: comparison of video-assisted thoracic surgery versus open approach. J Thorac Cardiovasc Surg. 2009;138:1318–25. Oizumi H, Kanauchi N, Kato H, Endoh M, Takeda S, Suzuki J, et al. Total thoracoscopic pulmonary segmentectomy. Eur J Cardiothorac Surg. 2009;36:374–7. Leshnower BG, Miller DL, Fernandez FG, Pickens A, Force SD. Video-assisted thoracoscopic surgery segmentectomy: a safe and effective procedure. Ann Thorac Surg. 2010;89:1571–6. Nakamura H, Taniguchi Y, Miwa K, Adachi Y, Fujioka S, Haruki T, et al. Comparison of the surgical outcomes of thoracoscopic lobectomy, segmentectomy, and wedge resection for clinical stage I non-small cell lung cancer. Thorac Cardiovasc Surg. 2011;59:137–41. Gossot D, Ramos R, Brian E, Raynaud C, Girard P, Strauss C. A totally thoracoscopic approach for pulmonary anatomic segmentectomies. Interact Cardiovasc Thorac Surg. 2011;12: 529–32. Yamashita S, Chujo M, Kawano Y, Miyawaki M, Tokuishi K, Anami K, et al. Clinical impact of segmentectomy compared with lobectomy under complete video-assisted thoracic surgery in the treatment of stage I non-small cell lung cancer. J Surg Res. 2011;166:46–51. Moroga T, Yamashita S, Tokuishi K, Miyawaki M, Anami K, Yamamoto S, et al. Thoracoscopic segmentectomy with intraoperative evaluation of sentinel nodes for stage I non-small cell lung cancer. Ann Thorac Cardiovasc Surg. 2012;18:89–94. Okada M, Mimura T, Ikegaki J, Katoh H, Itoh H, Tsubota N. A novel video-assisted anatomic segmentectomy technique: selective segmental inflation via bronchofiberoptic jet followed by cautery cutting. J Thorac Cardiovasc Surg. 2007;133:753–8. Yang CF, D’Amico TA. Thoracoscopic segmentectomy for lung cancer. Ann Thorac Surg. 2012;94:668–81. Smith CB, Kale M, Mhango G, Neugut AI, Hershman DL, Mandeli JP, et al. Comparative outcomes of elderly stage I lung cancer patients treated with segmentectomy via video-assisted thoracoscopic surgery versus open resection. J Thorac Oncol. 2014;9:383–9.
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Gen Thorac Cardiovasc Surg 49. Kato H, Oizumi H, Inoue T, Oba E, Nakamura K, Hayashi J, et al. Port-access thoracoscopic anatomical lung subsegmentectomy. Interact Cardiovasc Thorac Surg. 2013;16:824–9. 50. Kanzaki M, Kikkawa T, Shimizu T, Maeda H, Wachi N, Isaka T, et al. Presurgical planning using a three-dimensional pulmonary model of the actual anatomy of patient with primary lung cancer. Thorac Cardiovasc Surg. 2013;61:144–50. 51. Kanzaki M, Maeda H, Wachi N, Kikkawa T, Komine H, Isaka T, et al. Complete video-assisted thoracoscopic multi-subsegmentectomy based on patients’ specific virtual 3-D pulmonary models. Asian J Endosc Surg. 2013;6:110–5. 52. Okui M, Kohno M, Izumi Y, Asakura K, Nomori H. Combined subsegmentectomy for S(2)(b) (horizontal subsegment of the posterior segment) and S(3)(a) (lateral subsegment of the anterior segment) in the right upper pulmonary lobe. Gen Thorac Cardiovasc Surg. 2011;59:632–5. 53. Yoshimoto K, Nomori H, Mori T, Ohba Y, Shiraishi K, Ikeda K. Combined subsegmentectomy: postoperative pulmonary function compared to multiple segmental resection. J Cardiothorac Surg. 2011;6:17. 54. Oizumi H, Kanauchi N, Kato H, Endoh M, Suzuki J, Fukaya K, et al. Anatomic thoracoscopic pulmonary segmentectomy under 3-dimensional multidetector computed tomography simulation: a report of 52 consecutive cases. J Thorac Cardiovasc Surg. 2011;141:678–82. 55. Shimizu K, Nakano T, Kamiyoshihara M, Takeyoshi I. Segmentectomy guided by three-dimensional computed tomography angiography and bronchography. Interact Cardiovasc Thorac Surg. 2012;15:194–6. 56. Oizumi H, Endoh M, Takeda S, Suzuki J, Fukaya K, Sadahiro M. Anatomical lung segmentectomy simulated by computed tomographic angiography. Ann Thorac Surg. 2010;90:1382–3. 57. Nakashima S, Watanabe A, Ogura K, Higami T. Advantages of preoperative three-dimensional contrast-enhanced computed tomography for anomalous pulmonary artery in video-assisted thoracoscopic segmentectomy. Eur J Cardiothorac Surg. 2010;38:388. 58. Akiba T, Nakada T, Inagaki T. Three-dimensional pulmonary model using rapid-prototyping in patient with lung cancer requiring segmentectomy. Ann Thorac Cardiovasc Surg. 2013; (Epub ahead of print). 59. Akiba T. Utility of three-dimensional computed tomography in general thoracic surgery. Gen Thorac Cardiovasc Surg. 2013;61:676–84. 60. Akiba T, Morikawa T, Ohki T. Thoracoscopic lung segmentectomy simulated by a tailor-made virtual lung: computed bronchography and angiography. Thorac Cardiovasc Surg. 2013;61: 151–3. 61. Kamiyoshihara M, Kakegawa S, Morishita Y. Convenient and improved method to distinguish the intersegmental plane in pulmonary segmentectomy using a butterfly needle. Ann Thorac Surg. 2007;83:1913–4.
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62. Misaki N, Chang SS, Igai H, Tarumi S, Gotoh M, Yokomise H. New clinically applicable method for visualizing adjacent lung segments using an infrared thoracoscopy system. J Thorac Cardiovasc Surg. 2010;140:752–6. 63. Misaki N, Chang SS, Gotoh M, Yamamoto Y, Satoh K, Yokomise H. A novel method for determining adjacent lung segments with infrared thoracoscopy. J Thorac Cardiovasc Surg. 2009;138:613–8. 64. Tarumi S, Misaki N, Kasai Y, Chang SS, Go T, Yokomise H. Clinical trial of video-assisted thoracoscopic segmentectomy using infrared thoracoscopy with indocyanine green. Eur J Cardiothorac Surg. 2013; (Epub ahead of print). 65. Ishiguro T, Kumagai Y, Ono T, Imaizumi H, Honjo H, Suzuki O, et al. Usefulness of indocyanine green angiography for evaluation of blood supply in a reconstructed gastric tube during esophagectomy. Int Surg. 2012;97:340–4. 66. Ohtsuka T, Goto T, Anraku M, Kohno M, Izumi Y, Horinouchi H, et al. Dissection of lung parenchyma using electrocautery is a safe and acceptable method for anatomical sublobar resection. J Cardiothorac Surg. 2012;7:42. 67. Asakura K, Izumi Y, Kohno M, Ohtsuka T, Okui M, Hashimoto K, et al. Effect of cutting technique at the intersegmental plane during segmentectomy on expansion of the preserved segment: comparison between staplers and scissors in ex vivo pig lung. Eur J Cardiothorac Surg. 2011;40:e34–8. 68. Nomori H, Okada M. General knack of segmentectomy. In: Nomori H, Okada M, editors. Illustrated anatomical segmentectomy for lung cancer. 1st ed. Tokyo: Springer; 2012. p. 9–21. 69. Horinouchi H, Nomori H, Nakayama T, Kohno M, Izumi Y, Watanabe M, et al. How many pathological T1N0M0 non-small cell lung cancers can be completely resected in one segment? Special reference to high-resolution computed tomography findings. Surg Today. 2011;41:1062–6. 70. Nomori H, Mori T, Izumi Y, Kohno M, Yoshimoto K, Suzuki M. Is completion lobectomy merited for unanticipated nodal metastases after radical segmentectomy for cT1 N0 M0/pN1-2 nonsmall cell lung cancer? J Thorac Cardiovasc Surg. 2012;143: 820–4. 71. Gonzalez-Rivas D, Fieira E, Mendez L, Garcia J. Single-port video-assisted thoracoscopic anatomic segmentectomy and right upper lobectomy. Eur J Cardiothorac Surg. 2012;42:e169–71. 72. Hung MH, Hsu HH, Chen KC, Chan KC, Cheng YJ, Chen JS. Nonintubated thoracoscopic anatomical segmentectomy for lung tumors. Ann Thorac Surg. 2013;96:1209–15. 73. Pardolesi A, Park B, Petrella F, Borri A, Gasparri R, Veronesi G. Robotic anatomic segmentectomy of the lung: technical aspects and initial results. Ann Thorac Surg. 2012;94:929–34. 74. Deen SA, Wilson JL, Wilshire CL, Vallieres E, Farivar AS, Aye RW, et al. Defining the cost of care for lobectomy and segmentectomy: a comparison of open, video-assisted thoracoscopic, and robotic approaches. Ann Thorac Surg. 2014;97:1000–7.
CURRENT TOPICS REVIEW ARTICLE
Anatomical thoracoscopic segmentectomy for lung cancer Yoichi Ohtaki • Kimihiro Shimizu
Received: 31 March 2014 Ó The Japanese Association for Thoracic Surgery 2014
Abstract Minimally invasive surgery for lung cancer has seen considerable progress. A segmentectomy is less invasive than a lobectomy as it preserves lung parenchyma. The preservation of pulmonary function can reduce complications. The combination of a thoracoscopic approach with a segmentectomy should be less invasive, and retrospective studies have shown that the thoracoscopic approach is safe and feasible due to the lower postoperative mortality and complication rates as compared to an open thoracotomy. The validity of a segmentectomy for groundglass-opacity-type lung cancer has been demonstrated, and it has also been evaluated for small, predominantly solid, lung cancers. Two prospective studies of segmentectomy versus lobectomy for B2-cm non-small-cell lung cancer are now underway (CALGB 140503 and JCOG0802/ WJTOG4607L) and should clarify the role of segmentectomy. Regarding thoracoscopic segmentectomy, few retrospective studies have reported the oncological outcome for lung cancer and there is inadequate evidence regarding the long-term oncological outcome, although the perioperative complication rate and duration of hospital stay seem to be non-inferior to those of an open approach. For preoperative simulation, three-dimensional multidetector computed tomography (3D-CT) is essential for performing an atypical thoracoscopic segmentectomy safely. Preoperative 3D-CT angiography and bronchography (3D-CTAB) enable accurate identification of the venous branches in the
This review was submitted at the invitation of the editorial committee. Y. Ohtaki K. Shimizu (&) Department of Thoracic and Visceral Organ Surgery, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan e-mail: [email protected]
affected segment and the intersegmental vein. This review describes the surgical and oncological outcomes, utility of 3D-CTAB, and surgical techniques and procedure used for a thoracoscopic segmentectomy. Keywords Lung cancer Thoracoscopic Segmentectomy Video-assisted thoracic surgery (VATS) Three-dimensional computed tomography (3D-CT)
Introduction Minimally invasive surgery for the treatment of thoracic malignancies has been evolving since the 1990s. There are three methods of minimally invasive lung cancer surgery: thoracoscopic or robotic surgery with limited access to the thoracic cavity and minimal chest wall damage using a thoracoscope without a mechanical retractor and without rib spreading; segmentectomy, wedge resection, or sleeve resection with reduced resection of the pulmonary parenchyma; and selective lymph node dissection [1]. Currently, lobectomy and systemic lymph node dissection are considered the standard surgical procedure for patients with completely resectable clinical stage I nonsmall-cell lung cancer (NSCLC) [2]. Segmentectomy is used mainly for patients with metastatic lung tumors or primary lung cancer and reduced pulmonary function, or older patients. However, high-resolution computed tomography (HR-CT) allows us to detect small lung cancers. As a result, non-solid tumors appearing as groundglass opacities [3], suggestive of noninvasive lung cancer with a good prognosis, are being detected increasingly commonly. The validity of a segmentectomy for GGO or GGO-type lung cancer has been demonstrated [4–7], and it has also been evaluated as a treatment for small
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predominantly solid lung cancers. Correspondingly, the safety of thoracoscopic surgery or video-assisted thoracic surgery (VATS) has been established for segmentectomy for lung cancer. In Japan, segmentectomies for primary malignant pulmonary tumor were performed in 3176 (9.6 %) of the 33,112 lung cancer cases in 2010 and more than two-thirds of the segmentectomies were performed by thoracoscopic surgery [8]. In conjunction with these circumstances, this review describes the surgical and oncological outcomes, and surgical techniques and procedure, including the use of threedimensional computed tomography (3D-CT) angiography and bronchography (3D-CTAB) for thoracoscopic segmentectomy.
Benefits of segmentectomy over lobectomy for lung cancer In 1995, a prospective multi-institutional randomized trial conducted by the Lung Cancer Study Group (LCSG) showed that limited resection, including wedge resection and segmentectomy, was associated with a poorer overall survival and higher regional recurrence rate as compared with lobectomy [9]. Another study confirmed the increased survival risk of segmentectomy over lobectomy, especially for tumors larger than 3 cm [10]. Since then, anatomical segmentectomies have been reserved for patients with poor cardiopulmonary function or the elderly. However, the prospective LCSG study included many non-anatomical wedge resection cases, which could have led to the worse survival [11, 12]. Some reports have demonstrated that the oncological outcome of segmentectomy is not inferior to that of lobectomy, considering tumor diameter [13–24]. However, Whitson et al. found that lobectomy conferred a significant survival advantage compared with segmentectomy regardless of tumor size in a population-based analysis [25]. In a meta-analysis comparing segmentectomy with lobectomy for early stage NSCLC, Bao et al. reported that although lobectomy was superior to segmentectomy for Stage I or IA tumors, segmentectomy was equivalent to lobectomy for tumors B2 cm [26]. Two prospective studies of segmentectomy versus lobectomy for B2 cm NSCLC are now underway—the phase III randomized trials CALGB 140503 and JCOG0802/WJTOG4607L—and should clarify the role and feasibility of segmentectomy [27]. Furthermore, a prospective single-arm phase III trial for clinical T1N0 (B3 cm) lung cancer dominant with GGO is also now under survey (JCOG 1211), and is expected to clarify the feasibility of segmentectomy for GGO predominant lung cancer. One of the greatest benefits of segmentectomy compared with lobectomy is the improved postoperative pulmonary
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function due to the preservation of lung parenchyma [28, 29]. If curability and the local recurrence rate are secured, the preservation of pulmonary function will be a great advantage, especially for the elderly. In 2009, Kilic et al. reported that elderly patients who underwent segmentectomy had fewer major complications than those undergoing lobectomy (11.5 vs. 25.5 %) [13]. Although the difference was not significant (p = 0.24), the operative mortality was 1.3 % for the segmentectomy group and 4.7 % for the lobectomy group. The disparity in the complication and mortality rates between the groups might be explained by the fact that the majority of patients in both groups were operated on using an open approach. Since the surgical technique of thoracoscopic segmentectomy is more complex than thoracoscopic lobectomy [30], the complication rates and lengths of hospital stay were similar in both the thoracoscopic segmentectomy and thoracoscopic lobectomy groups [14, 31–33].
Advantage of a thoracoscopic segmentectomy over an open segmentectomy Consequently, segmentectomy has been shown to be less invasive than lobectomy, and the combination of a thoracoscopic approach with segmentectomy should be less invasive. Thoracoscopic or VATS segmentectomies have been described in the last 10 years [14, 21, 31, 32, 34–46]. Table 1 summarizes the patients’ characteristics and operative variables. In this review, thoracoscopic or VATS surgery includes both total thoracoscopic surgery and hybrid VATS surgery. A thoracoscopic segmentectomy was initially performed for relatively simple procedures, such as the left upper division, lingular division, and superior (S6) or basilar segment of the lower lobes [14, 34, 37], which are typical segmentectomies in Table 1. In a retrospective study comparing thoracoscopic surgery with an open approach, Atkins et al. showed that a thoracoscopic approach reduced the length of hospital stay [37]. Shiraishi et al. also found that patients undergoing a thoracoscopic segmentectomy had a significantly shorter postoperative hospital stay than those with an open thoracotomy, despite the significantly longer operating time [35]. Schuchert et al. reported that a VATS segmentectomy was associated with a decreased length of stay (5 vs. 7 days, p \ 0.001) and fewer pulmonary complications (15.4 vs. 29.8 %, p = 0.012) compared with an open segmentectomy [39]. Although these were retrospective studies, all of them showed that a thoracoscopic approach was safe and feasible due to the lower postoperative mortality and complication rates as compared to those of open thoracotomy. Consequently, a thoracoscopic approach might require a longer operation duration, but patients
2011
2011
2011
2012
Gossot [43]c
Yamashia [44]
Oizumi [54]c
Okada [21]
153
424
TS
OS
13 31
TS
90
73
102
52
38
OS
TS
TS
TS
TS
TS
50
26
OS
TS
15
43
30
41
31
TS
TS
TS
TS
TS
121
OS
29
104
OS
TS
48
52
TS
TS
34 25
TS
No. of patients
OS
Approach
75
76
72
70
69
72
67
66
72
57
64
65
62
69
63
65
70
70
59
62
65
72
69
Age (mean)
NA
NA
NA
NA
46
100
50
37
55
74
42
33
100
40
78
100
65
79
90
94
52
NA
NA
Typical (%)
a
NA
NA
NA
NA
54
0
50
63
45
26
58
67
0
60
22
0
35
21
10
6
48
NA
NA
Atypical (%)
b
Type of segmentectomy
§
c
b
a
NA
NA
167
191
257 ± 91
NA
129
216
NA
188 ± 54
140 ± 38
145 ± 55
NA
216
220
NA
143
136
130 ± 65
136 ± 45
155
204 ± 69
240 ± 72
Operating time (min)
NA
0.212
–
–
–
–
–
–
0.70
–
–
–
–
0.42
0.68
–
0.05
p value
NA
NA
3.2
2.8
4.8 ± 3.4
NA
1
NA
NA
3.3 ± 1.9
5.2 ± 3.0
2.8 ± 1.3
NA
1
3±2
2
NA
NA
3.7 ± 1
3.5 ± 4
3
6.1 ± 4.9
4.5 ± 3.2
Chest tube duration (days)
NA
0.487
–
–
–
–
–
–
0.001
–
–
–
–
NA
0.7
–
NS
p value
NA
NA
12.7
8.5
12.2 ± 8.2
3.8 ± 3.3
NA
NA
NA
5.6 ± 2.4
8.3 ± 6.1
3.5 ± 1.4
NA
NA
NA
4
7
5
6.8 ± 6
4.3 ± 4
NA
16.7 ± 7.7
12.7 ± 3.6
Length of stay (days)
Atypical includes all other types of segmentectomy
Comparison of the percentage of extended length of stay
Includes metastatic lung tumor and benign tumor cases
0.03
0.020
0.01
\0.05§
–
–
–
–
–
–
–
–
–
–
\0.001
–
0.01
p value
Typical includes segmentectomy of the left upper division (S1 ? S2 ? S3), lingular division (S4 ? S5), and superior segment (S6) or basilar segment of lower lobe segmentectomy
TS thoracoscopic segmentectomy, OS open segmentectomy, NA not available, NS not significant
2014
2010
Leshnower [41]
Smith [48]
2010
Sugi [32]
2013
2009
Oizumi [40]c
Tarumi [64]c
2009
Watanabe [38]
2012
2009
Shapiro [14]
2012
2009
Schuchert [39]
Soukiasian [17]
2007
Yamashita [31]
2007
Okada [46]
2004
Shiraishi [35]
Atkins [37]c
Year
Author
Table 1 Summary of thoracoscopic segmentectomy compared with open segmentectomy in the literature
39.2
26.1
16.1
15.4
19
37
9.8
6
NA
10.2
NA
NA
NA
7
10
26
33.9
26.0
34.5
31.3
13.5
20
11.7
Complications (%)
0.24
0.81
0.999
\0.05
–
–
–
–
–
–
NA
–
–
–
–
–
NS
p value
\7.0
3.1
0
0
0
NA
0
0
0
NA
2
0
0
NA
0
0
1.7
0
6.9
0
NA
0
0
Mortality (%)
NS
NS
–
–
–
–
–
–
0.27
–
–
–
–
0.50
0.14
–
NS
p value
Gen Thorac Cardiovasc Surg
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might have less wound pain than would be the case using an open thoracotomy approach. Regarding operative complications, the thoracoscopic segmentectomy group had lower rates of pulmonary complications and infection [39]. A segmentectomy is a complex procedure because it requires dissection of the intersegmental plane and peripheral branch of the segmental artery or vein. With a thoracoscopic approach, the procedure must be performed despite the limited view of the surgical field [33]. Yang and D’Amico indicated that surgeon’s experience should be added as a factor in future analyses [47], because the outcome might be affected by the surgeon’s skill. From an oncological perspective, few retrospective studies have compared the outcome of thoracoscopic segmentectomy versus thoracotomy segmentectomy [37, 39, 48]. Atkins et al. reported that the VATS segmentectomy group had an improved overall survival compared with the open thoracotomy group [37]. However, both groups included pulmonary metastases and benign tumors, and there was a disparity in tumor size. Using propensity score methods, Smith et al. reported that the overall and lung cancer-specific survival was similar between the two groups in Stage I lung cancer patients older than 65 years [48]. Schuchert et al. found no significant differences in local and systemic recurrence and survival between patients undergoing VATS and open segmentectomy for stage I NSCLC [39]. Therefore, thoracoscopic segmentectomy had an inadequate benefit in terms of the long-term oncological outcome. However, the perioperative complications and duration of hospital stay were not inferior to those of an open approach. Comparing the outcome according to the surgical approach used is difficult because of differences in the technique among institutions. Therefore, the surgical approaches should be evaluated in largescale multi-institution studies in combination with the mode or extent of resection.
Technical considerations for segmentectomy and the utility of three-dimensional computed tomography angiography and bronchography With improvements in surgical techniques, the resection of segments or subsegments other than those described above as typical segmentectomies has been reported; these are listed as atypical segmentectomies in Table 1 [13, 28, 31, 35, 38–41, 43, 44, 49–54]. Oizumi et al. classified thoracoscopic segmentectomy into three categories according to the degree of procedural difficulty, classifying segments that involve the dissection of multiple surfaces at acute angles, or contain a bronchial pulmonary artery deep within as ‘‘difficult’’, such as S7 (medial-basal segment), S9
123
(lateral-basal segment), and S10 (posterior-basal segment) [54]. Preoperative simulation using three-dimensional multidetector computed tomography (3D-CT) enables safe completion of a thoracoscopic segmentectomy [43, 49, 54– 60]. Previously, we described methods of identifying pulmonary vessel branches and segmental bronchi using 3DCT angiography and bronchography (3D-CTAB), and its benefits for segmentectomy [55]. Preoperative 3D-CTAB enabled us to identify the venous branches to the affected segment and intersegmental vein accurately, and to measure and plan the resection lines with an adequate surgical margin (Fig. 1). Figure 2 shows the 3D-CTAB image and operative findings of a segmentectomy case. The intrapulmonary anatomy, including the pulmonary artery, vein, and bronchus, varies greatly among patients. Consequently, the segmentectomy also varies because of the anatomical variation. Therefore, preoperative 3D-CTAB is essential for confirming the anomalous anatomy before a thoracoscopic segmentectomy [57]. Several procedures for recognizing the segmental plane have been reported. One technique for demarcating the segmental plane is to reinflate the ipsilateral lung temporarily after segmental bronchial ligation. Another is the selective jet ventilation method, which involves bronchoscopy into the involved segmental bronchus, as reported by Okada et al. [46]. We use this method because of its simplicity and safety. Kamiyoshihara et al. reported a method of inflating the involved segment using a butterfly needle [61]. Recently, Misaki et al. reported a method of identifying the segmental fissure using infrared thoracoscopy with indocyanine green (ICG) injection into a peripheral vein [62, 63], and confirmed its usefulness [64]. Oh et al. also reported a method using ICG injection into the involved segmental bronchus [65]. Each method has its advantages and disadvantages. For lung parenchymal dissection, several methods have been discussed, such as linear stapler and energy devices [46, 66, 67]. Electrocautery can be used to expand the residual lung parenchyma maximally and to obtain an accurate surgical margin [55]. A linear stapler is a comparatively simple method, and has been proposed to prevent prolonged air leakage, especially for emphysematous lung. After segmental resection, fibrin sealant and absorbable mesh for the resection line are useful for preventing prolonged postoperative air leakage [46, 68]. The most important aspect of a segmentectomy for lung cancer is securing a sufficient surgical margin. In cases of malignancy, the required surgical margin is greater than the tumor diameter or at least 2 cm of healthy lung tissue [46]. Furthermore, an HR-CT study reported that *30 % of c-T1aN0M0 NSCLC extends beyond one segment [69]. Therefore, segmentectomy of a single segment, which is
Gen Thorac Cardiovasc Surg Fig. 1 Three-dimensional multidetector computed tomography angiography and bronchography (3D-CTAB) images of the right a and left b lungs showing the pulmonary arteries (red) and veins (blue), and bronchi (yellow). The 3DCTAB image can be rotated as required
usually performed along the segmental vein with the aid of an inflation–deflation line, does not always provide an adequate surgical margin. Two methods can be used to obtain a sufficient surgical margin. One is used when the tumor is relatively close to the cutting line of the segmentectomy; the tumor is grasped within a ring-shaped forceps 3–5 cm in diameter and then the lung tissue is cut away from the forceps [70]. When the cutting line is beyond the intersegmental plane, a stapler is required to resect part of the neighboring segment. Alternatively, when preservation of the margin in a single-segment resection is difficult, an extended segmentectomy (a standard segmentectomy combined with resection of an adjacent segment or subsegment) is planned preoperatively using 3DCT and 2D-CT images [55]. The former method is technically easy, although it is difficult when the tumor cannot
be palpated or there is no access port for VATS beyond 3 cm. Therefore, we usually use the latter method for these situations.
New aspects of segmentectomy A novel technique to reduce the invasiveness of thoracoscopic segmentectomy is the single-port approach [71]. Gonzalez-Rivas et al. performed a single-port videoassisted thoracoscopic segmentectomy of the superior segment of the right lower lobe [72]. However, intensive training is necessary to perform single-port surgery and the size of the excised segment can be limited. A non-intubated thoracoscopic segmentectomy is another less-invasive method [72]. Hung et al. reported cases without intubation
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A
V1+2a+b
A3 B3 V3a+V1+2d
Furthermore, most of the reports reviewed were retrospective studies. The outcomes of two ongoing randomized controlled studies for B2 cm NSCLC (CALGB 140503 and JCOG0802/WJOG4607L) and one prospective single-arm trial for clinical T1N0 (B3 cm) lung cancer dominant with GGO (JCOG 1211) are expected in the near future. Conflict of interest All of the authors participated in this study and agreed on the content of this paper. None of them has any financial or other relationship that could lead to a conflict of interest.
V3c+V1+2c V3b
References
V4+5
B
V1+2a+b
A3 B3 V3a+V1+2d
V3c+V1+2c V3b
V4+5 Fig. 2 Left S1?2c ? S3a segmentectomy. a 3D-CTAB image at the hilum of the left upper lobe b Operative view of the patient. The hilum of the left upper lobe is exposed from the ventral to dorsal side to expose the superior pulmonary vein and arteries from the left main to the proximal site of the inter-lobar artery
using a combination of thoracic epidural anesthesia, intrathoracic vagal blockade, and target-controlled sedation [72]. Although the maneuver is complicated and requires a greater level of intraoperative attention, it might be useful in patients who are at high risk for general anesthesia. A robotic approach is an alternative procedure for segmentectomy [73]. However, robotic surgery will take a number of years to become widespread for reasons of cost and limited availability [74].
Limitations and future study This review included two types of thoracoscopic surgery: total thoracoscopic segmentectomy and hybrid VATS segmentectomy. Since they are very different approaches technically, it would be better to compare the outcome and operative data, although these would be influenced by the surgeon’s technique and the segment resected.
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