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Ann Thorac Surg 2004;77:1904-1910
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Minithoracotomy combined with mechanically stapled bronchial and vascular ligation for anatomical lung resection

Michael F. Szwerc, MDa*, Rodney J. Landreneau, MDb, Ricardo S. Santos, MDb, Robert J. Keenan, MDc, Gordon F. Murray, MDa

a Section of Cardiothoracic Surgery, West Virginia University School of Medicine and Morgantown West Virginia Hospital, Morgantown, West Virginia, USA
b Division of Thoracic and Foregut Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA
c Division of Thoracic Surgery, Allegheny General Hospital, Pittsburgh, Pennsylvania, USA

Accepted for publication December 1, 2003.

* Address reprint requests to Dr Szwerc, West Virginia University School of Medicine, Department of Surgery, Robert C. Byrd Health Sciences Center, PO Box 9238, Morgantown, WV 26506-9238, USA
e-mail: mszwerc{at}hsc.wvu.edu

Presented at the Forty-ninth Annual Meeting of the Southern Thoracic Surgical Association, Miami Beach, FL, Nov 7–9, 2002.


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Conclusions
 Acknowledgments
 Discussion
 References
 
BACKGROUND: The most appropriate approach to anatomic pulmonary resection has been debated with the advance of minimally invasive techniques and especially the common use of mechanical staplers. Video assisted surgery and muscle-sparing thoracotomy are established options of surgical approach for lung resection. We utilize a combined technique of vertical muscle sparing minithoracotomy and mechanical closure of the hilum structures to accomplish lung resection.

METHODS: From December 1995 through January 2002, 713 patients (mean age, 65 ± 11, 44.6% male) underwent anatomic pulmonary resection including 64 pneumonectomies, 514 lobectomies, and 135 formal segmental resections. Pulmonary resection was approached though a direct access, vertical, minithoracotomy (< 10 cm), and vascular ligation was performed with port-access endostapling instrumentation. Full mediastinal lymph node sampling was performed for primary lung cancer.

RESULTS: The average operative time was 55 minutes for lobectomy-formal segmentectomy and 62 minutes for pneumonectomy. An average of 3.6 staple applications were utilized to ligate the pulmonary vasculature (n = 2548 for 713 patients). Operative vascular complications included 5 minor intimal fractures, 1 posterior segmental arterial avulsion, and 1 staple misfiring for an adverse event rate during stapler application of 0.27%. Only one conversion to standard thoracotomy was necessary to control bleeding from the pulmonary vein. There were no intraoperative deaths.

CONCLUSIONS: Vertical minithoracotomy is a safe and expedited approach for anatomic lung resection. Direct visualization for dissection and effective pulmonary hilum mechanical closure with staplers were demonstrated. This approach is a reasonable option when a complete video-assisted surgery seems to be hazardous and a full open thoracotomy could represent an additional morbidity.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Conclusions
 Acknowledgments
 Discussion
 References
 
Complete anatomic resection remains the standard of treatment and provides the best chance of cure for early stage lung cancer [1]. Recent interest in minimally invasive techniques throughout all surgical disciplines is based on the premise that smaller surgical incisions lead to reduced postoperative pain, shorter hospitalization, and quicker functional recovery [2, 3]. Argument among thoracic surgeons continues regarding the appropriateness of "pure" video-assisted thoracic surgical approaches (VATS) to anatomic pulmonary resection for lung cancer [4].

Beyond the biases of individual surgeons, the surgical approach for anatomical lung resection is usually determined by the strategies necessary for control and dissection of the vascular hilum of the lung. Accordingly, VATS procedures are generally limited to resection of smaller peripheral lesions without hilar extension of the mass or associated adenopathy [5–7]. Large, central lesions are not generally considered amenable to VATS anatomic resection due to the difficulty in securing vascular control of the hilum. Open thoracotomy via a classic posterolateral, extensive lateral, or partial sternotomy approach is usually recommended for such lesions [8].

We describe the use of a "hybrid" surgical approach to anatomic pulmonary resection involving a mini-axillary vertical thoracotomy affording hilar control and direct visual inspection of pulmonary vasculature for dissection with conventional surgical instrumentation. Though this small incision (6 to 10 cm in length), the surgeon's hand can be introduced into the wound for palpation of the lung pathology and for direct tamponade of bleeding if necessary. Vascular ligation is accomplished with the use of the endostapler more commonly used for VATS techniques [9, 10].

Over the last 8 years we have utilized this mini-vertical axillary thoracotomy approach as our primary means for anatomic lung resection of small to moderate sized pulmonary nodules (masses) in lieu of total VATS or more extensive lateral or posterolateral thoracotomy approaches. Refinement in endostapling devices has contributed to our use of this "minithoracotomy" approach for anatomic lung resection as bronchovascular divisions and ligation can be safely accomplished with a shortening of the operative time and a decreasing of the technical difficulty associated with manual suture ligation of the pulmonary vasculature through such limited thoracotomy access.

The central focus of this report is toward validation of the safety and efficacy of this hybrid approach for anatomic pulmonary resection with particular emphasis on the utility of the endostapling technique for pulmonary vascular ligation [11].


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Conclusions
 Acknowledgments
 Discussion
 References
 
From December 1995 to January 2002, 713 consecutive patients underwent anatomic pulmonary resection at Allegheny General Hospital and West Virginia University Hospital. All procedures were accomplished through a minimal surgical access (vertical axillary minithoracotomy) with mechanical vascular stapling with the endoscopic stapling device (2.5-mm staple height). Bronchial ligation and division was variably accomplished with the endoscopic stapling device (3.5-mm staple height) for segmental bronchi and the TA-30 stapling device (4.5-mm staple height) for lobar or main stem bronchi. The mean patient age was 65 ± 11 years and 45% were male. Relevant preoperative clinical data, including pulmonary function data and comorbidities are depicted in Table 1. The decision to use this specific open technique was based upon surgeon preference. The common exclusion criteria identified among the surgeons were tumor size greater than 10 cm with hilar extension, or with extensive pleural adhesion identified by preoperative computed tomographic imaging (CT) of the chest. In these situations, alternative anterior (partial sternotomy) or classic posterolateral thoracotomy was utilized.


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  		Table 1. Preoperative Clinical Profile

 
All patients had pulmonary lesions with either histologic confirmation of malignancy by percutaneous biopsy or with characteristics highly suggestive for malignancy based upon CT and adjunctive positron emission tomographic scan (PET) data. Only patients who were operated on with the preoperative intent of formal anatomic resection, as opposed to wedge resection, were included in this analysis. Patient's data were reviewed regarding demographics, operative reports, and perioperative morbidity and mortality. Specific analyses of vascular complications during and after surgery were performed to study the safety of the method of endostapler vascular ligation during the performance of anatomic lung resection.

Operative technique
Double lumen endotracheal intubation with selective contralateral lung ventilation is obtained after successful induction of general anesthesia. Bronchoscopic confirmation of correct endotracheal tube position is performed before lateral positioning of the patient for thoracotomy. Inadequate ipsilateral pulmonary collapse disables the thoracic surgeon's ability to safely and expediently accomplish anatomic resection through this limited thoracotomy. Patients are positioned in the lateral decubitus position and supported with a beanbag and axillary roll. Preference in positioning is given to the anterior aspect of the hemithorax to gain access to the axilla. A vertical 5- to 10-cm thoracotomy access incision is created just below the axillary hairline in the anterior axillary line for upper lobe, hilar, and middle lobe lesions. Lower lobe tumors are approached through an incision that is slightly more posterior and inferior in location. When performing the upper axillary incision for upper lobe lesions, the "fingers" of the serratus anterior muscle are encountered lateral and perpendicular to the orientation of the pectoralis major muscle [12]. The aim is to enter the chest through the third or fourth intercostal spaces by separating the anterior aspects of the "fingers" of the serratus anterior at this level and then elevating the muscle belly to expose the underlying rib and intercostal musculature. Care is taken to avoid lateral separation of the serratus anterior muscle beyond the mid-axillary line to prevent inadvertent injury to the long thoracic nerve and vascular pedicle of the serratus anterior. It is occasionally necessary to notch the fourth rib posteriorly to allow for an approximate 5- to 6-cm opening between the ribs. Exposure is obtained by the placement of two small Finochetto retractors in perpendicular alignment with each other. One retractor is used to spread the ribs and the other to separate the anterior and posterior soft tissues of the wound (Fig 1).



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  		Fig 1. Incision (left) and operative exposure using two small Finochetto retractors (right).

 
For lower lobe lesions, the vertical incision is slightly inferior and posterior to that used for upper lobe processes so as to gain access to the pathology through the fourth or fifth intercostal spaces. The serratus anterior is identified and dissection is then carried out posterior to the entire belly of the muscle so as to result in anterior retraction of the entire muscle. The latissimus dorsi is retracted laterally and exposure of the ribs and intercostals is accomplished with division of the fascia posterior to the serratus anterior. For this exposure, rib notching of the fifth or sixth rib is routinely necessary to avoid rib fracture during rib spreading. Rib spreader orientation is similar to that used for the higher axillary incision described above.

Through this vertical minithoracotomy exposure, the surgeon's line of vision is directly at the hilum for upper lobe, middle lobe, and hilar lesions. The confluence of the major and minor fissures is directly visualized using the lower incision when approaching right lower lobe lesions. The lingular vasculature and midpoint of the major fissure is seen during left lower lobe resections. Access to the suprahilar region is without difficulty for nodal staging during the use of this lower incision. The hilar and lobar dissection is carried out using standard surgical instrumentation under direct vision through the wound. A lower mid-axillary line intercostal access site is established in the seventh or eighth intercostal space for subsequent introduction of the endostapler for pulmonary vascular ligation. A thoracoscope can be introduced through this lower intercostal access site during the procedure to periodically enhance intrathoracic illumination and to inspect areas out of direct view through the minithoracotomy. Additionally, coaxial endosurgical forceps ("Landreneau Mashers," Starr Medical Instruments, New York, NY; and Pilling Surgical, Horsham, PA) can be utilized through this intercostal access to facilitate pulmonary parenchymal retraction during the hilar dissection.

Once pulmonary vessels are dissected, the endostapler (ENDO GIA-30, U.S. Surgical Corp, Norwalk, CT) is introduced through a protecting 11-mm thoracoport (Snowden Pencer, Inc, Gasden, GA) and directed across the dissected vessel for the anticipated ligation. The endostapler can be introduced directly through the thoracotomy and across the vessel to be ligated if the angle is more appropriate. All pulmonary vessels, including the main pulmonary artery, are ligated using this technique (Fig 2). Care is taken to stabilize the shaft of the endostapler during the firing of the instrument to prevent torque about the vessel, which can lead to intimal fracture or tearing of the vessel. The surgeon should also keep a careful eye upon the advancement of the knife and staplers about the vessel during the endostapler application.



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  		Fig 2. Direct visualization of the pulmonary vessels (top) and ligation through a thoracoport, using a endostapler (bottom).

 
The method of bronchial ligation and division is dependent upon the size of the bronchus. We generally use the endostapler to accomplish transaction and closure of segmental bronchi during the course of anatomic segmentectomy. The endostapler with the 3.5-mm staple height is usually introduced through the accessory intercostal access site utilized for endostapling of the pulmonary vasculature. When lobectomy or pneumonectomy is being performed, we introduce a TA-30 stapler through the minithoracotomy wound to approach division and ligation of the bronchus.

Mediastinal lymph node sampling is routinely performed following resection of all primary lung cancers. The pleural space is drained with a 28F chest tube or a 19F Blake drain (Johnson and Johnson Medical, Inc, Arlington, TX). Two chest tubes are variably utilized after lobectomy when an increased risk of prolonged air leak is anticipated due to difficulty with interlobar dissection. After pneumonectomy, intrathoracic drainage is usually avoided unless there has been an unusually bloody intrathoracic dissection due to intrathoracic adhesions.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Conclusions
 Acknowledgments
 Discussion
 References
 
A total of 713 patients underwent anatomic pulmonary resection using this technique. Resections performed included 514 lobectomies, 64 pneumonectomies, and 135 formal segmental resections. The mean total operative time was 154.4 ± 69.6 minutes. This was calculated from induction of anesthesia to patient extubation following completion of the operative procedure. The actual surgical time required for anatomic resection was 55 minutes for a lobectomy-segmentectomy and 62 minutes for a pneumonectomy. The estimated blood loss was 263 ± 568 mL with a median blood loss of 200 (10 to 2,200 mL). Sixty-two percent of the tumors were pathologically staged as stage I or II with adenocarcinoma being the dominant histologic subtype.

The overall length of hospital stay was 6.7 ± 6.4 days with a median of 4.5 days and a range of 1 to 113 days. The mean intensive care unit (ICU) stay was 2.1 ± 7.4 days with a median of 1 day and a range of 0 to 79 days. There were no intraoperative mortalities. The 30-day mortality was 2.7%. The causes of death were respiratory failure (9), multisystem organ failure (4), cardiac arrest (2), cerebral vascular accident (2), and death after discharge from unknown reasons (2) patients.

There was an average of 3.6 endostapler applications per resection for a total of 2,567 stapler firings (Fig 3). Operative vascular complications included 5 intimal fractures, 1 posterior segmental artery avulsion, and 1 complete staple line failure occurring at attempted endostapler ligation and division of a lower lobe pulmonary vein during pneumonectomy. This required conversion to formal thoracotomy for vascular control and direct suture repair of the pulmonary vein. The intraoperative blood loss was estimated at 2,200 mL. Fortunately, this patient went on to have an uncomplicated postoperative course.



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  		Fig 3. Endostapler ligation (top) of the apical-anterior branch of the right pulmonary artery (bottom).

 
Atrial fibrillation was the most common general postoperative morbidity following resection, seen in 12.9% of patients (Table 2). Bleeding requiring reexploration occurred in 1 patient. The bleeding was identified to be from a retrobronchial arterial source. Superficial wound complications occurred in 8 patients (1.1%). Empyema requiring postoperative drainage occurred in 8 patients (1.1%).


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  		Table 2. Morbidity

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Conclusions
 Acknowledgments
 Discussion
 References
 
The vertical axillary thoracotomy was originally described by Browne in 1952 [13] and popularized by Noirclerc and colleagues [12]. This larger axillary vertical incision has been dubbed the "French incision" due to Noirclerc's dexterity as a thoracic surgical technician. This muscle sparing approach has been proven to be adequate for all the types of lung resection, including lung transplantation [6, 14–16].

Hilar ligation required for anatomic pulmonary resection has been performed utilizing automatic surgical staplers since their development in the Soviet Union in the 1950s. The successful smuggling of the technology into the United States later in that decade resulted in the description of the clinical utility of surgical mechanical stapling devices in the American literature in 1961 [17].

The development of an effective endostapling device in the late 1980s opened the door for minimally invasive anatomic pulmonary resection [18, 19]. Video-assisted thoracic surgical lobectomy can now be safely accomplished for selected pulmonary lesions by the thoracic surgeon with a good understanding of the pulmonary anatomy who has reasonable endosurgical experience [20–23].

In this light, reports of the utility and safety of endostapler use in pulmonary resection deserves review. Craig and Walker [24] expressed concern about vascular stapling during thoracoscopic pulmonary resection. They reported an endovascular stapling failure rate of 0.82% in a series of 62 patients who underwent VATS pulmonary resection. These failures can be generally attributed to user misuse of the technology. Although failure was attributed to misalignment of the anvil during endostapler manufacturing in this study, a more common reason for the stapler failures during pulmonary parenchymal wedge resection relates to inappropriate firing of the stapler across thick, indurated pulmonary tissues leading to staple line dehiscence and pulmonary parenchymal fracture.

In a recent study of 603 patients undergoing pulmonary resection, Asamura and colleagues [25] reported stapling failure in only one of 842 mechanical vascular divisions; this failure occurred in the superior pulmonary vein during video-assisted right upper lobectomy. The authors believed the reason for failure of the endostapler related to a misalignment of the cartridge during insertion of the stapler before firing. Interestingly, present endostaplers do not allow firing of the device by the surgeon unless the cartridge is properly aligned in the instrument.

In this series, an average of 3.6 endostapler applications were used to manage pulmonary vasculature during anatomic resection for a total of 2,567 firings. There was only one staple line failure, which occurred during division of the inferior pulmonary vein on a left pneumonectomy. It was believed that this endostapler failure was directly attributed to improper loading of the staple cartridge; however, the possibility of inappropriate positioning of the endostapler across the pulmonary vein and pericardium may have resulted in undue tension on the staple closure leading to acute dehiscence of the staple line. All additional injuries were related to excessive traction placed on pulmonary arterial branches when inserting or firing the endostapler.

The primary goal of VATS, and this approach, aims at reducing the procedural related morbidity related to anatomic pulmonary resection. The timeliness and safety of the procedure through either minimal incisional approach is also of importance. The combination of minithoratocomy and endostapler management of vasculature appears to be a reasonable hybrid approach to anatomic pulmonary resection, allowing for direct visual dissection and manual control of the pulmonary hilum. Importantly, this approach also allows for the education of thoracic surgical residents in the three-dimensional aspects of pulmonary anatomy in a setting of a safe, minimally invasive surgical approach to pulmonary resection.

Our series presents the operative results of 713 patients who underwent anatomic pulmonary resection utilizing a minithoracotomy and mechanical endostapler ligation of the pulmonary vasculature. The data demonstrated that it is feasible to perform pulmonary resection utilizing, exclusively, mechanical closure of vessels and bronchi. There were no intraoperative deaths and the overall 30-day mortality for that entire series of patients was (2.8%). None of the patients who died within 30 days had a death attributable to the technique of resection.


   Conclusions
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Conclusions
Acknowledgments
 Discussion
 References
 
The combination of the minithoracotomy performed through a vertical axillary incision with total mechanical stapled bronchovascular ligation seems to be safe and expeditious. A low number of complications were observed with this technique. This approach may minimize some of the current limitations of a "pure" VATS approach to anatomic pulmonary resection, and at the same time limit the incision related morbidity of the traditional thoracotomy.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Conclusions
 Acknowledgments
Discussion
 References
 
The following members of the Division of General Thoracic Surgery of the Allegheny General Hospital, Pittsburgh, PA, the West Virginia University School of Medicine, Morgantown, WV, and the Federal University of São Paulo, Brazil, are acknowledged for their efforts and contribution to this work: Richard H. Maley, MD, Neel K. Karne, BA, Tibetha Santucci, RN, Robin Macherey, RN, and Jose E. Succi, MD.


   Discussion
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Conclusions
 Acknowledgments
 Discussion
References
 
DR BRYAN F. MEYERS (St. Louis, MO): I enjoyed your presentation and I applaud you for showing that there is an alternative between a totally VATS lobectomy and a muscle-dividing thoracotomy for lobectomy. I think a lot of times when the less invasive approach gets touted, it is compared against the most invasive approach and thus accentuates the advantages. This paper shows nicely that there are many approaches that are somewhere in between. I have a couple of questions for you.

Seven hundred and thirteen patients over seven years is quite a large number of patients and quite a long period of time for a new procedure to be tried out. In addition, this was done at two different centers, and apparently this is a retrospective analysis, and I just wonder how two different centers with an unstated number of surgeons can agree upon the exact same technique over seven years and maintain the uniformity of the procedure that you are describing?

The other question is to point out the fact that you never mentioned the word conversion. Any kind of minimally invasive approach brings with it a risk of converting to the more invasive approach. All the VATS procedures that I would consent a patient for would include the possibility of converting, and I wonder, since there are zero conversions in this retrospective study, how you did your case-finding?

DR SZWERC: Thank you for your questions. These are not VATS procedures. These are just direct visualization minithoracotomy procedures using techniques that have been adopted by VATS resection. The beauty of this is you are doing the same operation as a standard thoracotomy. You just have less access.

So to get a group of surgeons to agree, part of the thing that makes it so intriguing and attractive to trainees who have learned this technique is that thoracotomy exposure is very quick, within two minutes you are down to where you need to start working, and closure is also very quick; you have no cases of seroma formation in your wounds.

Enlarging the incision is not necessary except in the one case, and it was a case of mine, where I had staple line failure on a pulmonary vein during a pneumonectomy and I just couldn't get down there to fix it.

Your second question?

DR SCOTT M. BRADLEY: In the interest of time, we are going to have to keep moving.

DR DAVID R. JONES (Charlottesville, VA): Mike, that was a very nice paper. Have you done any cost analysis to see whether this method of using the endostaplers is more cost effective than either just suture ligation or using the traditional staplers?

Second, I think the ability to use the endostaplers is determined by where your port access incisions are. How many port access incisions do you really need for the stapler? Do you use only one or two, and how do you really place those?

Finally, while you suggest that times are shorter and you are able to do the operation as a hybrid approach, based on your findings, are you willing to consider at a Phase III trial comparing this to a VATS lobectomy?

DR SZWERC: Thanks, David. Most of the time you need just one port to do the operation. The decision to place the port is usually based on once you look at where your pulmonary artery is and you have dissected it out, you just draw a straight line out through the skin and you figure out where a straight line is. These staplers do not reticulate, so you have just a straight shot, and it is usually an anterior port placed, and the second drainage port is sometimes not even used for thoracoscopy or placing a stapling device.

We have looked at a comparison of this type of technique to standard posterolateral thoracotomy. We don't have an interest right now in doing a comparison to pure VATS resection because this has kind of become our preferred technique, but I think it is an important thing to do.

The staplers are not cheap; each fire of that stapler is approximately $200 in our hospital. The beauty of using the stapler, however, is that it requires a lot less pulmonary dissection; you do not have to mobilize as much of a length of pulmonary vein. If you are going to use a TA stapler, you need more of a vein and it takes longer.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Conclusions
 Acknowledgments
 Discussion
 References
 

  1. Landreneau R.J., Sugarbaker D.J., Mack M.J., et al. Wedge resection versus lobectomy for stage I (T1N0M0) non-small cell lung cancer. J Thorac Cardiovasc Surg 1997;113:691-700.[Abstract/Free Full Text]
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