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Interact CardioVasc Thorac Surg 2009;8:316-320. doi:10.1510/icvts.2008.193672
© 2009 European Association of Cardio-Thoracic Surgery

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Institutional report - Pulmonary

Video-assisted thoracic surgery lobectomy preserves more latissimus dorsi muscle than conventional surgery{star}

Takahiro Karasakia, Jun Nakajimab,*, Tomohiro Murakawab, Takeshi Fukamib, Yukihiro Yoshidab, Masashi Kusakabeb, Hiroshi Ohtsuc and Shinichi Takamotob

a The University of Tokyo Faculty of Medicine, Tokyo, Japan
b Department of Cardiothoracic Surgery, The University of Tokyo Graduate School of Medicine, Tokyo, Japan
c Department of Clinical Trial Data Management, The University of Tokyo Graduate School of Medicine, Tokyo, Japan

Received 10 September 2008; received in revised form 26 October 2008; accepted 29 October 2008

{star} Presented at the 22nd Annual Meeting of the European Association of Cardio-thoracic Surgery, Lisbon, Portugal, September 14–17, 2008.

*Corresponding author. 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan. Tel.: +81-3-3815-5411; fax: +81-3-5684-3989.

E-mail address: nakajima-tho{at}h.u-tokyo.ac.jp (J. Nakajima).


    Abstract
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 
Video-assisted thoracic surgery (VATS) lobectomy for early lung cancer has become technically feasible. We sought to determine if VATS preserved chest wall muscle postoperatively better than thoracotomy. Consecutive patients who underwent lobectomy between 2004 and 2006 for clinical Stage IA non-small cell lung cancer through VATS (VATS group) or posterolateral thoracotomy (PLT group) at our institution were eligible for the study. The cross-sectional areas of bilateral latissimus dorsi muscle (LDM) at the lower end of the scapula were obtained by computed tomography preoperatively and one year after surgery. These were quantified with image analysis by two researchers in a blinded manner. Fourteen patients in the VATS group (mean age, 68 years; 8 men, 6 women) and 24 patients in the PLT group (mean age, 62 years; 14 men, 10 women) were assessed. Postoperative/preoperative ratios of the LDM cross-section areas on the surgical side were 89±20% (Mean±S.D.) in the VATS group and 57±16% in the PLT group (P<0.001). Those on the non-surgical side were 89±23% in the VATS group and 97±16% in the PLT group (P=0.23). We conclude that VATS may prevent atrophy of LDM on the surgical side better than conventional thoracotomy.

Key Words: Video-assisted thoracic surgery; Posterolateral thoracotomy; Latissimus dorsi muscle; Quality of life


    1. Introduction
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 
Lobectomy with lymph node dissection through video-assisted thoracic surgery (VATS) has recently become a treatment of choice for early stage non-small cell lung cancer (NSCLC) [1]. The invasiveness of pulmonary surgery and postoperative quality of life (QOL) have become major topics of the therapeutics of lung cancer.

Postoperative atrophy of the latissimus dorsi muscle (LDM) after conventional posterolateral thoracotomy has been reported by a few authors [2, 3]. However, to our knowledge, there is no report that quantitatively analyzes the atrophic change of LDM postoperatively. In this study, we measured the cross-section of LDM by computed tomography (CT), so as to quantify the atrophy of LDM, which may be one of the indicators of invasiveness of the thoracic wall muscles.


    2. Patients and methods
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 
Ethical approval was given by the Institutional Review Board of the University of Tokyo Hospital, and informed consent was obtained from all patients. Between January 2004 and December 2006, a lobectomy with lymph node dissections was performed on 73 consecutive patients with clinical Stage IA NSCLC in our hospital. Two patients were excluded because of a history of open thoracotomy, and another patient because of a history of thoracoscopy. Fifty-three patients underwent open thoracotomy, and 17, thoracoscopic surgery. Indications for VATS lobectomy for NSCLC in our institution were: age 75 years or more, severe systemic complications, or peripheral stage IA adenocarcinoma smaller than 2 cm in diameter. Of the 53 patients with open thoracotomy, 32 underwent conventional posterolateral thoracotomy (PLT) with transection, and later, resuturing of the LDM, and the other 21 were treated with muscle-sparing thoracotomy via the triangle of auscultation, or with anterolateral thoracotomy without transection of any major muscles.

The PLT consisted of an approximately 20-cm skin incision with a complete division of LDM. Serratus anterior muscle was preserved and the 5th rib was split to obtain an intrathoracic approach. In VATS, 3 or 4 access ports were inserted through 1~2 cm skin incisions in the side of the chest. Lobectomy was performed through these small incisions. One of these skin incisions was extended by 3–4 cm, and the lung lobe for resection was removed in a plastic bag without using a rib retractor. Patients in whom VATS was replaced intraoperatively with open thoracotomy were counted as open thoracotomy patients. Two patients whose incisions were extended to 8 cm and 10 cm, respectively, with the use of a small rib retractor were excluded from this study because they could be counted as thoracotomy patients.

In order to quantify the atrophy of the thoracic wall muscles after lobectomy, we measured the cross-section of LDM in preoperative and postoperative chest CTs of the patients with VATS and PLT. The preoperative CT was taken within three months of the surgery, and the postoperative CT was taken about one year after surgery. One patient with VATS and four with PLT were excluded from this study because their CTs did not meet the criteria above. Slice thickness and intervals were both set at 5 mm in all CT images. Window levels and widths were between 35 and 75 H.U., and between 250 and 350 H.U., respectively. The cross-section of the bilateral LDM was measured for each patient in both preoperative and postoperative CT. For the measurement of the cross-section of the LDM, the slice showing the lower tip of the ipsilateral scapula was chosen. The contour of the LDM on the selected CT image in JPEG format was drawn manually on the Microsoft Excel worksheet (Microsoft Corp., Redmond, WA, USA), and the area was calculated with a free macro program downloaded from the internet (lenaraf220) (http://www.vector.co.jp/download/file/win95/art/fh442375.html, Vector Japan Co, Ltd, Tokyo, Japan). Patient names, CT-scan dates and types of surgery were blinded, and the CT-scans were randomized. Measurements were made by two trained observers. The postoperative/preoperative ratio of the LDM cross-section was calculated to demonstrate atrophy of the LDM postoperatively.

Statistical analysis was performed using SAS version 9.1.3 (SAS Institute, Inc, Cary, NC, USA). The intraclass correlation coefficient of the preoperative LDM cross-section was calculated to assess the reliability of the measuring method performed by two observers. All continuous variables are expressed as mean±one standard deviation. Continuous data were analyzed with Student's t-test. Frequencies were compared using {chi}2-tests. All reported probability values are two-tailed, and P values <0.05 were considered statistically significant.


    3. Results
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 
The intraclass correlation coefficient of the preoperative LDM cross-section as determined by two observers was 0.953 and the reliability of the cross-section measurement method used in this study was statistically assured.

Four patients in the PLT group who were pathological stage III were excluded from this study because they received adjuvant chemotherapy before the one-year follow-up. Fourteen patients in the VATS group and 24 patients in the PLT group were assessed. Patient characteristics are shown in Table 1. No recurrence of the NSCLC was seen during the one-year postoperative follow-up. One patient in the VATS group was considered to have adenocarcinoma, according to the intraoperative pathological diagnosis, but the diagnosis was altered postoperatively to atypical adenomatous hyperplasia.


View this table:
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Table 1 Clinical data

 
Postoperative/preoperative ratios of the LDM cross-sectional areas of the surgical and non-surgical sides compared between the PLT and VATS groups are shown in Fig. 1 (surgical side; PLT: 57±16%, VATS: 89±20%, P<0.001) and Fig. 2 (non-surgical side; PLT: 97±16%, VATS: 89±23%, P=0.23). Although the reduction of the size of the LDM on the non-surgical side after VATS was slightly greater than that after PLT, the LDM on the surgical side was better preserved after VATS than after PLT.


Figure 1
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Fig. 1. Postoperative/preoperative ratios of latissimus dorsi muscle on the surgical side (P<0.001).

 

Figure 2
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Fig. 2. Postoperative/preoperative ratios of latissimus dorsi muscle on the non-surgical side (P=0.23).

 
Of 38 patients who were eligible in this study, 14 were 70 years old or more and 24 were younger. Comparisons of the postoperative/preoperative ratios of LDM on the non-surgical side between older patients and younger patients are shown in Fig. 3 (younger patients: 101±10%, older patients: 82±25%, P=0.016). There was a tendency for LDM on the non-surgical side in the older patients to be more atrophic than that in younger patients.


Figure 3
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Fig. 3. Comparison of postoperative/preoperative ratios of latissimus dorsi muscle on the non-surgical side between older patients and younger patients (P=0.016).

 

    4. Discussion
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 
Surgical therapy for lung cancer in the form of a lobectomy with lymph node dissections using thoracoscopy is feasible for selected, highly experienced surgeons. Swanson and colleagues stated that thoracoscopy has recently become a treatment of choice for patients with stage I NSCLC [1]. This technique may be justified if (i) it is safely performed, (ii) the postoperative prognosis is not worse than that for conventional thoracotomy, and (iii) the postoperative QOL is better preserved than that offered by conventional thoracotomy.

Several studies have shown that postoperative morbidity and mortality of VATS lobectomy were as good as, or rather better than, those of conventional thoracotomy [4, 5]. The hilar and mediastinal lymph node dissections are controversial from the oncological viewpoint, but some recent reports indicate that the lymph node dissections through thoracoscopy can satisfactorily be done thoroughly [6, 7], probably because of evolution of the technique and more thorough training of surgeons. The long-term postoperative survival rate of patients with NSCLC undergoing VATS lobectomy has been reported to be equal to that of patients undergoing thoracotomy [5–7].

The postoperative QOL has been evaluated by respiratory functional reserve, shoulder movement, wound pain, duration of hospital stay, and biological markers such as c-reactive protein and interleukin-6 [4, 7–11]. The majority of issues favorably assisted the thoracoscopy, especially in the early postoperative period. In this study, we focused on postoperative atrophic change in the latissimus dorsi muscle as an indicator of the performance status of patients undergoing lung cancer surgery.

We used our own criteria, based on previous studies, and our own clinical experience, as indications for VATS lobectomy for NSCLC: age 75 years or more, severe systemic complications, or small Stage IA adenocarcinoma. Therefore, older patients and patients with more severe systemic complications were more likely to undergo VATS. From the analysis of the LDM on the non-surgical side, we have shown that this muscle tends in the elderly to be more atrophic than in younger patients after a lobectomy. We may therefore say that age is a major factor in postoperative atrophy of the chest wall muscles. In this study, the reduction of the size of the LDM on the non-surgical side after VATS was slightly greater than that after PLT. This could perhaps be explained by the larger number of patients with systemic complications and slightly higher age of the patients in the VATS group. Nonetheless, the atrophy of LDM on the surgical side was more severe after PLT. We may assume that VATS preserves more LDM than conventional thoracotomy.

Animal experiments and clinical studies have shown that denervation of the muscle may be the major cause of atrophy [12, 13]. There are several reports which suggest that VATS has a better prognosis for short-term postoperative pain than PLT [4, 7–9]. However, it is reported that there is no significant difference in long-term postoperative pain between VATS and PLT [9], which indicates that postoperative disuse due to pain is less likely to be the cause of the atrophy of LDM. On the other hand, scientific support is lacking, short-term postoperative pain may delay the rehabilitation of shoulder movement after PLT, which also may promote LDM atrophy.

A questionnaire survey by Li et al. in 2003 showed that there was no significant difference between PLT and VATS three months after surgery in terms of various activities of daily living (ADL) such as putting on clothing [10]. On the other hand, it is well known that the muscle strength and cross-section are usually correlated [14], and LDM strength reduction due to LDM atrophy is inevitable – but, of course, the muscle strength required in ADL is small, although not, for example, in more energetic shoulder and arm exercise. Further study is needed regarding the long-term prognosis for shoulder function.

Limitations of this study include the small patient number and the non-randomized, retrospective nature of the study. Although consecutive patients were evaluated in this study, we used our own criteria, stated above, when recommending VATS lobectomy as a treatment of choice. As a result, background of each group was different in some aspects. Another limitation of this study was that we could not show the clinical relevance of LDM atrophy to postoperative QOL. A prospective study with a larger number of patients is required to confirm the larger LDM atrophy and deterioration of QOL after conventional thoracotomy.

There were other limitations in the method of LDM measurement used in this study. From our experience, the LDM has a relatively large cross-section on a CT slice showing the inferior tip of the scapula, and this is why we chose this particular slice when measuring the cross-section of LDM. However, this measuring method involved several problems. First, elevation of the arms may induce a positional change of the inferior tip of the scapula or deformation of the LDM; and second, a relationship between dissection of the serratus anterior muscle (SAM) and a postoperative winged scapula has previously been suggested [15], and displacement of scapula may have changed the conditions of measurement, which may have skewed the result. In our institution, we almost always preserve SAM during PLT, and so the displacement was not a big issue in most of the cases in the present study, but was still seen in some.


    5. Conclusions
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 
This study showed that VATS prevents LDM atrophy of the operative side better than conventional thoracotomy does. In terms of the atrophy of LDM, which is a major chest wall muscle, it can be said that VATS is less invasive of the thoracic wall. Further prospective studies are needed to show the clinical relevance of atrophy of the chest wall muscles to deterioration of postoperative QOL.


    Conference discussion
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 
Dr. S. Cassivi (Rochester, Minnesota, USA): I have two questions. You may have dealt with it a bit in your conclusions. You have shown very elegantly how you have got a smaller latissimus dorsi on the ipsilateral side a year after the surgery. Is there any functional data to show any difference in the use of that muscle?

Dr. Karasaki: As I said, one of the limitations of this study was that we couldn't show the clinical relevance. So we didn't perform the study regarding the muscle strengths or the respiratory function. So my answer is no.

Dr. Cassivi: Since you're bringing the patients back a year later for a CT-scan, you might want to do some strength testing just to see if there is any benefit or any difference afterwards.

Dr. Karasaki: That is the next study I'm thinking about.

Dr. Cassivi: Fair enough. The second question is a little bit unrelated to the nature of your study, but it's something that maybe you can enlighten us all on. Whenever we have cross-cultural exchanges like this where we see how surgery is done in one part of the world and another, it raises some questions. One of the reasons we do VATS is to get patients back to their community and back into the swing of things, so to speak. I understand that your length of stay after VATS is 14 days?

Dr. Karasaki: Yes. Actually, I was also surprised to see this number. In Japan the patients are staying in the hospital definitely longer than in the other countries and the government is now working on a shorter hospital stay. I was surprised to see this number because now the hospital length of stay is shorter than the number I showed.

Dr. C. Saldarriaga (Medellin, Colombia): I have a concern. Do you use low-dose radiation chest CT, and do you have an approval by your board in your hospital for this kind of investigation? I have a concern about the radiation from the CT for this investigation. By the way, I would like to invite you to use more muscle-sparing thoracotomies than dorsal section thoracotomies.

Dr. Karasaki: What you mean is if we used the same machine?

Dr. Saldarriaga: With the chest CT do you use low-dose radiation, like for screening? If you use the radiation from a conventional CT for this investigation, it is very dangerous.

Dr. Karasaki: I don't know the exact number, but the CT-scan conditions were all the same and the slice interval was 5 mm, and so I think it was the same conditions as screening.

Dr. J. Nakajima (Tokyo, Japan): I am a co-author of the paper.

Actually, we routinely follow-up the patients after surgery, performing the chest and the abdominal CT-scan every six months for two years to examine recurrence of the lung cancer. Data of this study were obtained from these CT images. Thus the patients have not undergone additional radiation exposure for this study.

Dr. L. Lang-Lazdunski (London, UK): I have two short questions. First, you said for your VATS lobectomy you make 3 or 4 1 cm to 2 cm incisions. I would be interested to know how you get your lobe out through a 1 cm to 2 cm incision.

Second, did you use the same analgesia in open and VATS patients? Did you use an epidural catheter or PCA or a paravertebral block? That could obviously influence your results. And in patients who had VATS, I suppose you didn't divide the latissimus dorsi pedicle.

Dr. Karasaki: The first question about the size of the incision, when retracting the resected lobe, we extend the incision to about 4 cm to 6 cm, on average.

Dr. Lang-Lazdunski: And the analgesia was the same in both groups?

Dr. Karasaki: In most of the cases we used an epidural besides the general anesthesia.

Dr. Lang-Lazdunski: For both groups?

Dr. Karasaki: Yes, for the postoperative pain.

Dr. N. Novoa (Salamanca, Spain): I would like to make a comment. I think that now we have sufficient knowledge to do surgery through very small incisions, and your work will help people to not use such huge thoracotomies as they previously were using. But my real comment goes to not only muscle-sparing thoracotomies, but also, do you think there is a necessity to do the whole procedure as a closed procedure, and before removing the lobe, you need to open one of the skin incisions a little bit? You can do the complete procedure through a 3 cm, 4 cm, 5 cm little incision without any difference and not doing difficult things through VATS, a completely closed procedure. It was just a comment.


    Acknowledgements
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 
The authors are very grateful to: Yusuke Suka, The University of Tokyo Faculty of Medicine, for help with data collecting; Masataka Taguri, Department of Biostatistics, The University of Tokyo School of Health Sciences and Nursing, for help with statistical analyses; and Mr C.W.P. Reynolds for his careful proofreading of the English of this manuscript.


    References
 Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusions
 Conference discussion
 Acknowledgements
 References
 

  1. Swanson SJ, Herndon JE 2nd, D'Amico TA, Demmy TL, McKenna RJ Jr, Green MR, Sugarbaker DJ. Video-assisted thoracic surgery lobectomy: report of CALGB 39802 – a prospective, multi-institution feasibility study. J Clin Oncol 2007;25:4993–4997.[Abstract/Free Full Text]
  2. Goodman P, Balachandran S, Guinto FC Jr. Postoperative atrophy of posterolateral chest wall musculature: CT demonstration. J Comput Assist Tomogr 1993;17:63–66.[Medline]
  3. Frola C, Serrano J, Cantoni S, Casiglia M, Turtulici I, Loria F. CT findings of atrophy of chest wall muscle after thoracotomy: relationship between muscles involved and type of surgery. AJR Am J Roentgenol 1995;164:599–601.[Abstract/Free Full Text]
  4. Muraoka M, Oka T, Akamine S, Tagawa T, Nakamura A, Hashizume S, Matsumoto K, Araki M, Tagawa Y, Nagayasu T. Video-assisted thoracic surgery lobectomy reduces the morbidity after surgery for stage I non-small cell lung cancer. Jpn J Thorac Cardiovasc Surg 2006;54:49–55.[CrossRef][Medline]
  5. Whitson BA, Andrade RS, Boettcher A, Bardales R, Kratzke RA, Dahlberg PS, Maddaus MA. Video-assisted thoracoscopic surgery is more favorable than thoracotomy for resection of clinical stage I non-small cell lung cancer. Ann Thorac Surg 2007;83:1965–1970.[Abstract/Free Full Text]
  6. Sugi K, Kaneda Y, Esato K. Video-assisted thoracoscopic lobectomy achieves a satisfactory long-term prognosis in patients with clinical stage IA lung cancer. World J Surg 2000;24:27–30.[CrossRef][Medline]
  7. Watanabe A, Koyanagi T, Obama T, Ohsawa H, Mawatari T, Takahashi N, Ichimiya Y, Abe T. Assessment of node dissection for clinical stage I primary lung cancer by VATS. Eur J Cardiothorac Surg 2005;27:745–752.[Abstract/Free Full Text]
  8. Nagahiro I, Andou A, Aoe M, Sano Y, Date H, Shimizu N. Pulmonary function, postoperative pain, and serum cytokine level after lobectomy: a comparison of VATS and conventional procedure. Ann Thorac Surg 2001;72:362–365.[Abstract/Free Full Text]
  9. Landreneau RJ, Mack MJ, Hazelrigg SR, Naunheim K, Dowling RD, Ritter P, Magee MJ, Nunchuck S, Keenan RJ, Ferson PF. Prevalence of chronic pain after pulmonary resection by thoracotomy or video-assisted thoracic surgery. J Thorac Cardiovasc Surg 1994 Apr;107:1079–1085.[Abstract/Free Full Text]
  10. Li WW, Lee RL, Lee TW, Ng CS, Sihoe AD, Wan IY, Arifi AA, Yim AP. The impact of thoracic surgical access on early shoulder function: video-assisted thoracic surgery versus posterolateral thoracotomy. Eur J Cardiothorac Surg 2003;23:390–396.[Abstract/Free Full Text]
  11. Nakajima J, Takamoto S, Kohno T, Ohtsuka T. Costs of videothoracoscopic surgery versus open resection for patients with of lung carcinoma. Cancer 2000;89:2497–2501.[CrossRef][Medline]
  12. Küllmer K, Sievers KW, Reimers CD, Rompe JD, Müller-Felber W, Nägele M, Harland U. Changes of sonographic, magnetic resonance tomographic, electromyographic, and histopathologic findings within a 2-month period of examinations after experimental muscle denervation. Arch Orthop Trauma Surg 1998;117:228–234.[CrossRef][Medline]
  13. Duchateau J, Declety A, Lejour M. Innervation of the rectus abdominis muscle: implications for rectus flaps. Plast Reconstr Surg 1988;82:223–228.[Medline]
  14. Morris CB. The measurement of the strength of muscle relative to the cross section. Res Q 1948;19:295–303.[Medline]
  15. Fiddian NJ, King RJ. The winged scapula. Clin Orthop Relat Res 1984;185:228–236.[Medline]




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