Ann Thorac Surg 2003;75:1990-1997
© 2003 The Society of Thoracic Surgeons
Review
Changes in the treatment of Pancoast tumors
Frank C. Detterbeck, MDa*
a Division of Cardiothoracic Surgery, Department of Surgery, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
* Address reprint requests to Dr Detterbeck, Division of Cardiothoracic Surgery, CB# 7065, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7065, USA
e-mail: fdetter{at}med.unc.edu
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Abstract
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Our understanding of superior sulcus tumors has evolved over time. The unique feature of Pancoast tumors is their location, in which the anatomy poses limitations to resection. Many resections are found to be incomplete, and the majority of recurrences have involved local failure. New surgical approaches allow greater flexibility according to tumor location and may improve these outcomes. Furthermore, new approaches permit complete resection of tumors involving vertebral bodies or the neural foramina. Traditionally, preoperative radiotherapy has been used, but a recent prospective phase II study suggests that preoperative concurrent chemoradiotherapy improves the rate of complete resection, local recurrence, and intermediate-term survival.
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Introduction
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It has been more than 160 years since a patient with a tumor of the superior sulcus of the lung was first described by Hare [1], and it has been nearly 80 years since clinical and radiographic features of this tumor were described by Dr Henry Pancoast, a radiologist, in 1924 [2]. These tumors have been named Pancoast tumors or Pancoast-Tobias tumors after further descriptions of their features by these authors in 1932 [3, 4]. Preoperative radiation and resection has been the standard treatment for approximately 40 years [5]. Our understanding of the anatomy, biology, and outcomes after treatment of these tumors has evolved over time. Several concepts regarding these tumors are changing as a result.
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Definition
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The classic definition of a Pancoast tumor was a cancer involving the apex of the chest that caused pain radiating down the arm because of involvement of the lower roots of the brachial plexus and caused Horner’s syndrome because of involvement of the stellate ganglion [2–4]. Currently, however, most reports of these tumors include any patient with a tumor in the typical location of Pancoast tumors, regardless of whether Horner’s syndrome or pain radiating down the arm is present [6–14]. The spectrum of disease implies that there will be patients with the full syndrome caused by tumor involvement of the brachial plexus, whereas others have a tumor encroaching on structures at the apex of the chest but without malignant invasion to the extent of causing nerve dysfunction.
A review of larger series of Pancoast tumors published during the last decade suggests that a fairly consistent definition is being used, even though a formal definition has not been explicitly cited [6–10, 15]. Based on this review of recent publications, a formal definition for Pancoast tumors is proposed: A Pancoast tumor is a lung cancer arising in the apex of the lung that involves structures of the apical chest wall. Involvement of the chest wall only at the level of the second rib or lower should not be considered to meet the criteria for involvement of the apex of the chest. The chest wall involvement may be limited to invasion of the parietal pleura, or may extend deeper to involve the periostium or the bone of the upper ribs or apical vertebral bodies, or it may include invasion of the subclavian vessels, the nerve roots of the brachial plexus, or the stellate ganglion. An apical tumor involving only the visceral pleura (T2) and not the chest wall by clinical staging should not be classified as a Pancoast tumor. However, it seems reasonable to include tumors that are thought to involve the chest wall by clinical criteria, even if this is eventually found not to be the case by pathologic examination after resection (and usually after preoperative radiotherapy).
Some authors have distinguished between tumors of the superior sulcus and apical lung tumors that involve the apical chest wall structures secondarily when the tumor becomes more advanced [16, 17]. However, this represents an arbitrary distinction along a continuum and is therefore a characteristic that is impossible to define. Furthermore, although a tumor may be larger, it is not necessarily of a more advanced stage (with regard to nodal involvement or distant metastases). Finally, if a resection is contemplated, the issues are the same regarding invaded apical chest wall structures. Therefore, this distinction does not appear to be useful.
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Anatomy
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A more detailed awareness of the anatomy of the thoracic inlet allows an appreciation for nuances among superior sulcus tumors that affect the optimal operative approach. The thoracic inlet can be divided into anterior, middle, and posterior components (Table 1)
[9]. The anterior component lies anterior to the insertion of the anterior scalene muscle onto the first rib, the middle compartment extends from there to the posterior border of the middle scalene muscle, whereas the posterior compartment lies behind the middle scalene muscle [9]. Tumors in each of these locations give rise to slightly different clinical presentations and involve different technical considerations for the surgeon.
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Tumor biology
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It was traditionally believed that the biology of Pancoast tumors was different from that of other non–small cell lung cancers (NSCLC), in that these tumors had a strong propensity to local invasion and a diminished incidence of spread through lymphatic or hematogenous routes [5]. However, the data do not support this belief. Pathologic N2 (pN2) involvement is consistently found in 10% to 20% of resected patients, who were likely to have been selected on the basis of presumed lack of lymph node involvement [18]. This is similar to the incidence of pN2 disease in other peripheral clinical stage I or II (cI, II) NSCLC [19, 20]. Furthermore, the available data show that survival is better when resection of a Pancoast tumor involves a lobectomy rather than a wedge resection alone. This also suggests that the biology of Pancoast tumors is not different than that of NSCLC in general.
The unique feature of Pancoast tumors appears not to lie in the tumor biology but rather in the anatomy of the region in which these tumors occur. Because these tumors involve the chest wall by definition, it is logical that these patients usually present with local rather than systemic manifestations of lung cancer. Furthermore, the local extension of Pancoast tumors involves structures that are difficult to approach technically and that limit the extent of resection if major long-term disability is to be avoided. Therefore, it is difficult to accomplish a complete resection (R0 resection) of these tumors. Thus, the technical aspects of the anatomy of this region represent the most prominent unique feature of Pancoast tumors.
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Staging
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Little attention has been given to defining the appropriate extent of staging of Pancoast tumors, despite the fact that staging of NSCLC in general has been studied extensively. Traditionally, confirmation of the status of the mediastinal nodes by mediastinoscopy and imaging for distant metastases has not been routine in patients with a Pancoast tumor. The incidence of unsuspected N2 disease suggests that further assessment of the mediastinum by means of mediastinoscopy or perhaps positron emission tomography would be worthwhile. The 5-year survival of less than 10% in patients with a Pancoast tumor and pN2,3 involvement underscores the importance of identifying these patients preoperatively [6, 21]. The incidence of unsuspected distant metastatic disease in patients with Pancoast tumors who have a normal clinical evaluation is unknown. Nevertheless, with the advent of more aggressive treatment approaches (preoperative chemoradiotherapy or more extensive resections), an argument can be made to pursue more aggressive extrathoracic staging even in patients without symptoms of distant metastases (eg, imaging of the brain and a bone scan or a positron emission tomography scan).
Ipsilateral supraclavicular nodal involvement is classified as N3 disease. However, there is some evidence that such involvement in patients with a Pancoast tumor may not preclude long-term survival [6, 22]. Ipsilateral supraclavicular node involvement in these patients may have a prognostic importance more akin to that of N1 disease. This warrants careful further study, as the data available at this time are very limited.
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Treatment
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Surgical principles
Resection of a Pancoast tumor should ideally involve a lobectomy along with the affected area of chest wall. Previously, a wedge resection of the lung was often deemed to be acceptable. However, it has become clear that lobectomy results in better survival than wedge resection, consistent with the changing view that the biological behavior of Pancoast tumors is similar to that of NSCLC in general. This is substantiated by a 5-year survival of 60% versus 33% for lobectomy versus wedge resection among patients with complete resection (p = 0.06) [6]. Because these data are retrospective they may be subject to selection bias, although the inclusion of only patients who underwent complete resection should minimize this effect. Others have found no survival difference between lobectomy and wedge resection but have not attempted to control for other factors [14].
Although the importance of achieving a complete resection is intuitively obvious, surgeons have often not been aware of how frequently a resection of a Pancoast tumor is found to be incomplete, and have not necessarily had the willingness or the experience to undertake a more difficult resection to achieve negative margins. In approximately one third of resections of a Pancoast tumor, a complete resection is not achieved [18]. Moreover, the survival after an incomplete resection is similar to that after no resection at all [6, 21, 23–25]. The fact that local recurrences account for the majority of recurrences after resection of Pancoast tumors stands in stark contrast to the experience after resection of NSCLC in other locations and underscores the unique anatomical issues presented by superior sulcus tumors. A greater awareness of the relatively high rate of incomplete resection coupled with advances in surgical techniques should lead to a higher proportion of complete resections and better rates of local control, at least in more experienced centers.
Surgical approaches
The classic approach to a Pancoast tumor, popularized by Paulson and Shaw [5], involved a high posterior thoracotomy with division of the muscles between the scapula and spinous processes to expose the upper ribs posteriorly (Fig 1).
This approach allows excellent exposure of the posterior chest wall including the transverse processes and thoracic nerve roots. It also allows standard exposure of the pulmonary hilum. However, resection of the subclavian vessels is difficult with this approach. Furthermore, visualization of the apex of the chest is poor until the tumor and chest wall have been mobilized, making assessment of the appropriate extent of resection difficult.
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Fig 1. High posterior thoracotomy. Incision extends around tip of scapula, midway between posterior edge of scapula and spinous processes, up to level of C7 (dark dashed line). (From Dartevelle P, Macchiarini P. Resection of superior sulcus tumors. In: Kaiser LR, Kron IL, Spray TL, eds. Mastery of cardiothoracic surgery. Philadelphia: Lippincott-Raven Publishers, 1998:257–65 [9], by permission of Lippincott Williams & Wilkins.)
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Several other approaches have been developed. Some authors have described a hook incision that encompasses the classic posterolatereral thoracotomy incision but curves upward anteriorly toward the sternoclavicular joint [23, 26]. This allows extensive retraction of the scapula, especially if the major and minor pectoral muscles are divided. Exposure of the chest wall and anterior apical chest structures such as the subclavian vessels is better than with the classic posterior approach. However, the muscles of the shoulder girdle are disrupted extensively.
Dartevelle and colleagues [27] described an anterior transcervical–thoracic approach (Fig 2),
which involves an incision along the anterior border of the sternocleidomastoid muscle that continues laterally over the clavicle. The sternocleidomastoid muscle is divided and the medial half of the clavicle is resected. Variations of this approach include simple division of the midportion of the clavicle with subsequent reconstruction with plates and screws [28], or disarticulation of the sternoclavicular joint and inferolateral retraction of the clavicle without clavicular resection [29]. After division of the internal jugular vein and anterior scalene muscle, the anterior transcervical–thoracic incision affords excellent exposure of the brachial plexus and subclavian vessels. Resection of the posterior portions of the upper two to three ribs can also be accomplished, but resection of lower ribs is difficult and pulmonary resection by means of a conventional lobectomy is awkward. It may sometimes be necessary to make a separate posterior incision to complete the resection [27].
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Fig 2. Anterior transcervical–thoracic and cervicothoracic transmanubrial incisions. Incision along anterior border of sternocleidomastoid muscle is carried either directly over clavicle (transcervical incision) or two fingerbreadths below inferior border of clavicle (transmanubrial incision). (From Dartevelle P, Macchiarini P. Resection of superior sulcus tumors. In: Kaiser LR, Kron IL, Spray TL, eds. Mastery of cardiothoracic surgery. Philadelphia: Lippincott-Raven Publishers, 1998:257–65 [9], by permission of Lippincott Williams & Wilkins.)
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A variation of the anterior transcervical–thoracic approach is the cervicothoracic transmanubrial approach (Fig 2), in which a similar skin incision is made except that the horizontal portion courses two fingerbreadths below the clavicle [30]. The manubrium is divided down the middle and then laterally into the second intercostal space. Division of the first costal cartilage allows the clavicle and ipsilateral half of the manubrium to be retracted while preserving the sternocleidomastoid muscle. This approach improves exposure of the subclavian vessels and allows easier resection of the upper anterior chest wall while providing similar exposure to the brachial plexus as compared with the anterior transcervical approach. The main advantage of the transmanubrial approach is that it preserves the function of the clavicle as well as the pectoral and sternocleidomastoid muscles.
A transsternal approach (Fig 3)
using a median sternotomy with an extension just above the clavicle provides good exposure of tumors involving the anterior upper chest wall, particularly if the subclavian artery or the superior vena cava (SVC) is involved [31]. The clavicle is usually left in continuity with the sternum; alternatively the anterior portion of the clavicle can be resected if necessary. It is usually necessary to divide the sternocleidomastoid muscle and the internal jugular vein. The apical chest structures including the vessels and brachial plexus can be clearly exposed and a lobectomy can easily be accomplished. Anterior division of ribs is straightforward, and lateral rib division is easily performed through a small axillary incision. However, division of posterior ribs is more difficult unless the ribs are disarticulated from the vertebral bodies and transverse processes.
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Fig 3. Anterior transsternal approach. The incision involves an upper median sternotomy (1), an extension into the anterior 4th intercostal space (2), and a transverse incision above the clavicle at the base of the neck (3). (From Dartevelle P, Macchiarini P. Resection of superior sulcus tumors. In: Kaiser LR, Kron IL, Spray TL, eds. Mastery of cardiothoracic surgery. Philadelphia: Lippincott-Raven Publishers, 1998:257–65 [9], by permission of Lippincott Williams & Wilkins.)
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Several authors have described using a combination of incisions, particularly for the resection of more extensive tumors [27, 32, 33]. Such a combination may include an anterior approach, a posterolateral thoracotomy to divide the necessary hilar structures, and a posterior approach to divide appropriate vertebral elements. With increasing experience, however, it appears that most of these more extensive resections can be accomplished with an anterior and a midline posterior approach alone without the addition of a posterolateral thoracotomy [32, 33].
Contraindications and limitations to surgery
Traditionally, involvement of the subclavian vessels, the neural foramina, or a vertebral body have been considered as relative contraindications to surgery in patients with a Pancoast tumor. This position may have partly been a reflection of the lack of well-developed techniques for resection of these structures. Until recently, only anecdotal cases of such resections had been reported, and detailed results were not available. For example, 2 of 9 patients were reported to be alive 2 years after resection of the subclavian vessels in two studies [10, 11]. Only 2 of 22 patients with vertebral body involvement were alive 5 years after partial vertebral resection, although the tumor involved only a very small portion of the vertebral body [6]. Thus the available experience was very limited.
In 1993, Dartevelle and colleagues [27] described an anterior approach to Pancoast tumors, which made resection of the subclavian vessels much easier. These authors reported a 5-year actuarial survival of 30% in 12 patients with Pancoast tumors who underwent subclavian vessel resection and reconstruction [27]. Another recent paper has reported a 5-year survival of 40% in 25 patients with subclavian vessel involvement [14]. In this latter study, many of the patients underwent resection through a posterior approach, although approximately 60% underwent "resection" of the vessels along a subadvential plane only. These papers illustrate that, with appropriate techniques in experienced centers, good long-term survival can be achieved after resection of a Pancoast tumor with subclavian vessel involvement.
The advent of centers with specialized experience in spine stabilization has led to the development of surgical techniques for resection of vertebral bodies with malignant involvement. All gross tumor was resected, albeit not en bloc with the lobectomy and chest wall specimen, in one series of 17 patients with a Pancoast tumor involving vertebral bodies (Fig 4)
[34]. Of the patients, 7 underwent total vertebrectomy, 7 a partial vertebrectomy, and the remaining 3 a resection of the transverse process and the bony structures around the neural foramina. The approach was primarily through a posterolateral thoracotomy, although a few patients underwent a combined anterior and posterior incision. Good intermediate term survival (2-year survival 54%) was seen, particularly in the 65% of patients in whom a complete resection with negative margins was achieved (2-year survival 80%; Fig 5). Local recurrence was found in all patients who had a positive final margin and in only 9% of patients with a negative margin, but the follow-up was relatively short [34].
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Fig 4. Multilevel thoracic vertebrectomy and laminectomy, reconstruction with methylmethacrylate, placement of anterior locking plate and screw construct, and posterior fixation with hooks and rods. (Reprinted with permission from The Society of Thoracic Surgeons [Ann Thorac Surg 1999, 68, 1778–85] [34].)
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Fig 5. Overall survival according to status of surgical margins in patients undergoing resection of a lung cancer involving the vertebral bodies. (Neg. = negative; Pos. = positive.) (Reprinted with permission from The Society of Thoracic Surgeons [Ann Thorac Surg 1999, 68, 1778–85] [34].)
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Two centers in Paris have outlined approaches that allow en bloc resection of a tumor involving the intervertebral foramina or the vertebral bodies [32, 33]. Fadel and colleagues [32] reported on 17 patients with involvement of at least two intervertebral foramina from superior sulcus tumors who underwent resection through a combined anterior cervicothoracic and posterior approach. None of these patients had vertebral body or spinal canal invasion by magnetic resonance imaging. The anterior approach allowed lateral division of the involved nerve roots, ribs, partial midline division of the appropriate vertebral bodies, and complete lobectomy. The vertical posterior midline incision was used to perform unilateral division of the involved lamina and nerve roots proximal to the dorsal ganglion. After completion of the midline osteotomy of the vertebral body, the specimen was removed and posterior spine stabilization was accomplished. The resection was complete in all cases. The median survival was 26 months, the 5-year survival rate was 20%, and local recurrence was seen in only 18% of patients [32].
Grunenwald and colleagues [33] reported 19 patients who underwent an en bloc resection of the lung and vertebral bodies (hemivertebrectomy in 15, complete vertebrectomy in 4, with a median number of 3 vertebral bodies resected). This was accomplished primarily using a cervicothoracic transmanubrial approach in addition to a midline posterior incision. Complete resection was achieved in 79% of patients and 19% of patients were found to have N2,3 involvement. The rate of local recurrence was 47% overall and 33% in patients who underwent an R0 resection. The median survival was 24 months and the 5-year survival was 14%. As in the other series of major vertebral resections, there was no operative mortality, although postoperative complications were common [33].
These series clearly illustrate that resection of a Pancoast tumor with vertebral body involvement, using advances in surgical techniques, can result in long-term disease-free survival. Further refinement of these techniques may allow increases in the local control and survival rates. Such extensive resections should only be undertaken in centers with expertise in spinal surgery and superior sulcus tumors, and with a sustained and focused commitment to treating such patients.
Multimodality therapy
The traditional approach to superior sulcus tumors has been preoperative radiotherapy followed by resection, although this standard was established 40 years ago solely on the basis of encouraging short-term survival as compared with historical controls [5]. Recently, preoperative concurrent chemotherapy and radiotherapy has been explored by several groups [15, 35–37], involving both single-institution experiences [15, 36, 37] and a prospective multiinstitutional phase II Intergroup protocol [35]. In the latter study the induction chemoradiotherapy was well tolerated, with a mortality of 2% and with approximately 10% of patients experiencing a nonhematologic toxicity of grade 3 or higher [35]. The rate of complete resection was 92% as opposed to an average of 66% among historical series of conventional treatment [18, 35]. Approximately one third of the operated patients demonstrated a pathologic complete response (pCR) to the induction treatment and in another one third only microscopic foci of viable tumor remained [35]. Local recurrences accounted for only 23% of recurrences as opposed to an average of 58% among historical series of conventional treatment [18, 35]. The 2-year survival rate for all patients entered into the study was 55% as opposed to an average of 42% among historical series of conventional treatment (Fig 6)
[18, 35]. The smaller single-institution reports have also found similar high rates of complete resection, pathologic complete response, local control, and survival [15, 36, 37].
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Fig 6. Overall survival by T stage for all eligible patients with follow-up in a prospective trial of preoperative chemotherapy and radiotherapy. (From Rusch VW, et al, J Thorac Cardiovasc Surg; 2001;121:472–83 [35], with permission.)
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The consistency of the data regarding preoperative chemoradiotherapy and regarding preoperative radiotherapy alone is convincing that preoperative chemoradiotherapy represents a new standard of care for patients with Pancoast tumors. No randomized data are available comparing these approaches, but the rarity of these tumors precludes such a study. Theoretical support for the use of preoperative concurrent chemoradiotherapy is provided by the randomized data from non-Pancoast stage IIIa,b NSCLC, which demonstrates that concurrent chemoradiotherapy results in better local control and better survival than does radiotherapy alone [38–41]. Therefore it appears justified to adopt preoperative concurrent chemoradiotherapy as the new standard for Pancoast tumors, a disease in which the ability to achieve local control has been the primary issue.
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Future directions
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Although the understanding of the biology and treatment of Pancoast tumors has evolved significantly, it is clear that more progress is needed. It is always difficult to guess the direction in which further developments will take us. However, a rational strategy toward further research requires that we at least define which issues should be explored next. Issues to investigate at this point include the role of more aggressive surgery in cases of more extensive involvement of the brachial plexus; the role, timing, and sequence of systemic chemotherapy in addition to preoperative concurrent chemoradiotherapy; and the role of prophylactic cranial irradiation (PCI).
Advancements in surgical techniques for Pancoast tumors now permit resection of subclavian vessels and even vertebral bodies, but extensive involvement of the brachial plexus remains a contraindication to resection. However, supportive care or treatment with radiotherapy alone often eventually lead to a functionless arm as a result of further tumor growth. It may be reasonable to explore the role of a more extensive surgical procedure such as a forequarter amputation. It is possible that the morbidity of such an operation is offset by the eventual morbidity of further tumor growth if this is not done—as well as by a chance of cure.
The experience with preoperative concurrent chemoradiotherapy and resection has demonstrated that the majority of relapses with this approach involve distant sites, in contrast to the experience with preoperative radiotherapy alone [35]. Thus the concurrent chemoradiotherapy has resulted in the expected improvement in local control, and further improvements in survival must involve attempts to decrease the incidence of distant recurrences. The addition of further systemic chemotherapy is supported by randomized studies of patients with non-Pancoast NSCLC demonstrating that systemic chemotherapy decreases the incidence of distant recurrences [42, 43]. The ability to deliver adjuvant chemotherapy after resection of a lung cancer has consistently been poor [44]. Therefore it may be best to add several cycles of chemotherapy either before or after the concurrent chemoradiotherapy, although this would delay resection of the Pancoast tumor.
Prophylactic cranial irradiation (PCI) may be a useful addition to preoperative chemoradiotherapy in patients with a Pancoast tumor, based on the observation that the brain was the most common site of first recurrence and 41% of all recurrences involved only the brain in the Intergroup study [35]. There is ample evidence among patients with SCLC that PCI reduces the incidence of subsequent brain metastases, although a survival advantage is realized only in patients who have a complete response to treatment [45]. Generally PCI is well tolerated, and it could be given postoperatively to patients with a Pancoast tumor after a complete resection has been accomplished.
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Conclusions
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Treatment of patients with Pancoast tumors continues to be a formidable challenge. However, progress is being made in the understanding of the anatomy and biology of this disease, and new treatment approaches are being developed that hold promise for a better outlook for these patients. A choice of incisions provides options that have the potential to increase the rate of complete resection. New techniques allow resection of structures that were previously considered unresectable. The addition of concurrent chemotherapy to the traditional approach of preoperative radiotherapy and surgery appears to be a significant advance in terms of local control and intermediate term survival. These successes have allowed new issues to present themselves. Although a superior sulcus tumor was first described more than 160 years ago and the classic treatment of radiotherapy followed by resection has been used for more than 40 years, the pace of progress in the treatment of this disease is accelerating dramatically.
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Abstract
Introduction
