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J Thorac Cardiovasc Surg 1998;115:286-295
© 1998 Mosby, Inc.
GENERAL THORACIC SURGERY |
From the Thoracic Service, The Memorial Sloan-Kettering Cancer Center, New York, N.Y.
Read at the Twenty-third Annual Meeting of The Western Thoracic Surgical Association, Napa, Calif., June 25-28, 1997.
Received for publication July 8, 1997; revisions requested July 28, 1997; revisions received Sept. 23, 1997; accepted for publication Sept. 23, 1997. Address for reprints: Michael E. Burt, MD, PhD, Thoracic Service, The Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
| Abstract |
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| Introduction |
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Malignant tumors encountered in this region, whether primary or metastatic, represent a heterogeneous group of tumors that tend to be locally aggressive and frequently recur after surgical resection.
1-5 The risk of injury to important neurovascular structures has made the prospect of radical resection formidable, even though complete resection offers the best hope for cure.
6 Multiple techniques have been described to provide access to this region. However, because no technique is without its drawbacks, the debate regarding the optimal approach continues.
The purpose of this report is threefold. First, we describe the "hemi-clamshell" approach for the resection of both primary and metastatic tumors of the cervicothoracic junction. This approach, consisting of a partial median sternotomy combined with an anterior thoracotomy and neck incision, provides exceptional exposure for the resection of tumors in this area, as well as for resection of associated structures such as the lung and vertebral body. Second, the morbidity and mortality of this technique are evaluated. Third, survival data are presented for a series of 42 patients with both primary and metastatic tumors of the cervicothoracic junction who underwent the hemi-clamshell approach for the resection of their tumors.
| Methods |
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The hemi-clamshell approach was performed as follows. The patient is placed supine and undergoes general anesthesia. After intubation with a double-lumen endobronchial tube, the ipsilateral upper extremity is tucked at the side to facilitate manipulation of the chest wall without fracturing the clavicle. The contralateral upper extremity is abducted and the neck is extended with the head turned to the contralateral side. The patient is then prepared and draped in sterile fashion from the chin to the umbilicus. Fig. 1 demonstrates the optimal position of the patient.
An anterolateral thoracotomy incision is made from the sternum to the anterior axillary line. Electrocautery is used to divide the soft tissue of the chest wall, and the fourth intercostal space is entered. Care is taken to divide the pectoralis major proximal to its insertion onto the ribs to allow reapproximation without tearing of this muscle. The ipsilateral lung is collapsed and the pleural cavity is explored for findings that would preclude resection (diffuse pleural metastases). Once the decision to proceed has been made, the intercostal space is opened out to the midclavicular line and the skin incision is continued cephalad up the middle of the sternum and the anterior border of the ipsilateral sternocleidomastoid muscle. Fig. 1
depicts the skin incision in its entirety.
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The tumor present in the cervicothoracic junction can now be readily dissected free from the surrounding neurovascular structures. En bloc resection of neighboring involved structures such as the vertebral bodies, ribs, veins, arteries, nerves, and thyroid is now possible because of this wide exposure. The pulmonary hilum is also easily dissected, allowing for various anatomic lung resections to be performed without the need for a separate thoracotomy incision.
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| Results |
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En bloc resection of the tumor with surrounding invaded structures was readily achieved through the hemi-clamshell approach in all but two patients. A separate posterolateral thoracotomy was required in these two patients (5%) to facilitate removal of tumor invading the posterior chest wall. All gross tumor was resected in 35 patients (83%); four patients had a microscopically positive margin. Table III lists the structures and organs involved by tumor that required resection along with the mass. No structures were inadvertently sacrificed.
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| Discussion |
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The posterior approach to bronchogenic carcinomas in the superior sulcus as described by Paulson
12 provides adequate exposure for resection of apical lung tumors invading the posterior aspect of the ribs and cervicothoracic junction but makes resection of anterior apical tumors difficult, especially in the presence of extensive extrathoracic invasion. Access to the pulmonary hilum is excellent, facilitating any type of pulmonary resection that may be necessary. Surgical access for the resection of bronchogenic carcinoma invading the thoracic inlet has also been described by Dartevelle and associates
13 through an L-shaped transcervical incision. With this approach, however, control of the pulmonary vessels at the hilum and chest wall resection below the second rib are difficult, necessitating a separate posterolateral thoracotomy in 20 of 29 patients (69%) in this series. In addition, this approach involves the resection of the medial half of the clavicle, which contributes to shoulder instability, weakness, and deformity.
14,15 Access for complete mediastinal lymph node dissection, a necessary component of many oncologic operations, is also very limited.
Macchiarini and coworkers
6 described an identical technique for the resection of both primary and metastatic nonbronchogenic tumors of the thoracic outlet in 14 patients. Four of these patients again required the performance of additional incisions to facilitate exposure for tumor resection, and the medial half of the clavicle was resected in all patients. One patient died after the operation and there was one late death resulting from progressive disease, but the remaining 12 patients were without evidence of disease at a median follow-up of 3.4 years.
Nazari
16 recently reported a modification of the anterior transcervical approach (Dartevelle technique) in which the clavicle is not divided. Although shoulder stability may be improved by wiring the clavicle back to the manubrium, this approach is still hampered by the exposure problems characteristic of the Dartevelle technique.
Grunenwald and Spaggiari
14 agree with Nazari concerning the disadvantages of resecting the clavicle when resecting tumors of the cervicothoracic junction. These authors describe an anterior approach similar to that described by Nazari except that the sternoclavicular joint is maintained and the manubrium is divided to "open" the access to the thoracic inlet. The advantage of this technique is improved shoulder stability attained by leaving the sternoclavicular joint and the muscular attachments of the clavicle intact. However, in their series of eight patients, four required an additional posterolateral thoracotomy to facilitate the performance of pneumonectomy and vertebrectomy.
We have previously reported the hemi-clamshell technique for the exposure and resection of spinal tumors from the C4-T3 levels, as well as for a small series of soft tissue tumors at the cervicothoracic junction.
17,18 A similar technique has also been described for the resection of both mediastinal tumors with extensive hemithoracic involvement
19and superior sulcus lung tumors.
20 The present report represents the largest series ever reported for the resection of tumors in this area by any approach. The hemi-clamshell technique has several advantages over the approaches previously described by other authors. First, exposure of the pulmonary vessels at the hilum is excellent, facilitating the performance of major anatomic pulmonary resections, which were required in 19% of the patients in this series, including three pneumonectomies. Second, there is no limit on the size of the chest wall resection that can be performed by means of the hemi-clamshell approach. Third, the clavicle is not divided and the sternoclavicular joint is left intact, which diminishes postoperative discomfort and improves shoulder stability and appearance. Fourth, the hemi-clamshell approach is far better than any other described technique for the performance of mediastinal lymph node dissection, a necessary part of many tumor resections.
The only disadvantage of the hemi-clamshell approach in the resection of tumors of the cervicothoracic junction is the exposure of the posterior chest wall and neural foramina. This problem is shared by the other anterior approaches to these tumors. As a result, we continue to use the traditional posterior approach described by Paulson
12 to remove superior sulcus tumors invading the posterior aspect of the first rib, reserving the hemi-clamshell technique for anterolateral tumors. In the uncommon instance in which a tumor involves the posterior apical chest wall and invades the cervicothoracic junction structures anteriorly as well, two separate incisions may be necessary. We found this to be the case in two (5%) of our 42 patients.
The hemi-clamshell approach has been criticized by some because of questionable ability to perform vertebral body resections and because of the possibility of postoperative flail chest.
14,20 In our series of 42 patients, we successfully performed seven vertebral body resections and the flail chest phenomenon was not seen in any patients. Figs. 2
and 3
demonstrate the excellent access to the cervicothoracic vertebral bodies.
In summary, we describe the hemi-clamshell technique for the resection of primary and metastatic tumors involving the cervicothoracic junction and report survival data on the largest series of patients treated for tumors in this area. As described, this technique has significant advantages over approaches previously published in the thoracic surgical literature. The complication rate is low and the mortality rate is zero in this series of 42 patients. Long-term survival is encouraging provided that a complete resection can be performed.
| Appendix: Discussion |
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It is remarkable that no deaths occurred in this series of 42 patients. Although the neurovascular structures are at a major risk for this procedure, no neurovascular structures were apparently damaged. The overall actuarial 5-year survival was 67.4%, but the 5-year actuarial survival for the primary tumors was a remarkable 73.6%. These results are as good as anyone could ever hope for, and the authors should be congratulated.
I have a few questions. You have described the operation and your results but have not mentioned what criteria you use to determine that these tumors are resectable. Does this series reflect all patients that you see with cervicothoracic tumors, or is this a very selected group of patients? What do you do with patients with arm, shoulder, or back pain and probable brachial plexus involvement? Also, what do you do with the patient with probable mediastinal adenopathy? How do you handle the patient who probably has unresectable disease and therefore cannot be cured and who may have also been irradiated in the cervicothoracic area?
Dr. Korst. We use the preoperative computed tomographic scan to determine which tumors are resectable; however, in many cases, operative exploration is needed. The best patient for this approach is a patient who has a tumor that tends to be anterior on the computed tomographic scan. In the case of a superior sulcus tumor that appears to be invading the posterior aspect of the first rib, we will do the posterolateral approach as described by Paulsen. However, if the tumor is more anterior and lateral, we will use the hemi-clamshell approach.
Dr. Cannon. One of the issues that arises is that these tumors are not encountered until there is pain, and there is often pain associated with involvement of the brachial plexus. If the brachial plexus were involved in some "minor" fashion, so that only a portion needed to be removed, understanding the fact that some arm paralysis would be associated with the procedure, would you do that?
Dr. Korst. We have taken the T1 nerve roots; we have not had patients in whom we have needed to take more of the brachial plexus.
Dr. Cannon. What do you do if the patient has obvious mediastinal lymphadenopathy?
Dr. Korst. All patients have a preoperative computed tomographic scan to evaluate the mediastinum. If bulky nodes are present, a tissue diagnosis is obtained. If diffuse mediastinal metastases are present, resection is usually not attempted.
Dr. Cannon. One of the issues that arises is the fact that some of these tumors are induced by radiation therapy and often develop in an irradiated area. What we often encounter is a patient who has a lot of pain in this area, has an obvious tumor, and probably has unresectable disease. How do you handle those problems? These are very difficult problems that are going to become increasingly prevalent, because a lot of these patients with breast cancer and lymphomas were cured of the initial disease, perhaps 20 years ago, and now have a major problem that we have to treat.
Dr. Korst. We do an exploratory operation if we think the disease is resectable. Two of the patients in this series actually had postradiation tumors, and both had good results after exploration and resection.
Dr. Cannon. One last question: Have you had to turn down a number of patients because of inoperability, large tumors, or extensive involvement of the brachial plexus?
Dr. Korst. I do not have that data.
Dr. Cannon. The point I am trying to make is that sometimes an arm has to be amputated because of the involvement of this area, and that is a real problem.
Dr. John R. Benfield (Sacramento, Calif.). I do not recall your mentioning the right recurrent laryngeal nerve. Did you ever have to sacrifice that as part of the planned part of the operation? Second, were there any instances in which that nerve was damaged when you had not intended it to be?
Dr. Korst. We did not have to intentionally sacrifice the recurrent laryngeal nerve. We did have one instance in which there was a traction injury to the nerve, because the vocal cord paralysis was self-limited.
Dr. Richard G. Fosburg (Del Mar, Calif.). My curiosity is piqued by the fact that a third of the patients in this series had what would be characterized as limited pulmonary resections, one segmentectomy and 14 wedge resections. Has there been a change in your philosophy about the treatment of malignant pulmonary disease at Memorial Sloan Kettering?
Dr. Korst. The anatomic pulmonary resections are basically performed for the primary lung cancers. If the tumor is not a primary lung cancer but invades the lung, a wedge resection is performed.
Dr. Fosburg. In your abstract you indicated that there are 28 primary tumors, 12 of which were lung tumors. Are you implying that the 12 patients who had lung tumors were not subjected to wedge resection?
Dr. Korst. The majority of the patients with lung cancers had anatomic resections. There were instances in which wedge resection or segmentectomy was performed.
Dr. James B. D. Mark (Stanford, Calif.). Just a technical question. All of find ourselves having to extend incisions when we have started with one approach. Do you plan this particular incision right from the start, or have you done, perhaps, a sternotomy or a thoracotomy and then had to extend it into the other portion of the incision?
Dr. Korst. We plan it right form the start. However, we start the procedure with an anterior thoracotomy, because we want to eliminate the possibility of pleural disease that would make us have to stop the operation. After the thoracotomy, we go up the sternum and up the neck.
Dr. Mark. Do you think you could remove some of the anterior tumors with a standard sternotomy and not have to extend into the chest? You determine this on the computed tomographic scan, I presume.
Dr. Korst. Yes, the computed tomographic scan determines the approach. These tumors extend from the chest up into the thoracic inlet, and I think that area is hard to safely approach through just a sternotomy, even with a neck extension.
The exposure with this approach, being able to raise the chest wall up like a flap, is phenomenal. We have had no added morbidity from adding the thoracotomy to the sternotomy.
Dr. Mark. Can we call this maximally invasive surgery?
Dr. Korst. Yes.
Dr. Paul F. Waters (Los Angeles, Calif.). In the patients with lung cancer, do you evaluate the lymph nodes before taking them out, or do you do mediastinoscopy first?
Dr. Korst. The primary lung cancers we treat like superior sulcus tumors. Most of them are staged with cervical mediastinoscopy.
Dr. Waters. Do they get the standard preoperative therapy?
Dr. Korst. The decision to give preoperative radiotherapy is surgeon- and patient-specific.
| Footnotes |
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| References |
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