DOI: 10.1148/rg.282075709
RadioGraphics 2008;28:551-560
© RSNA, 2008
Imaging of Non–Small Cell Lung Cancer of the Superior Sulcus
Part 1: Anatomy, Clinical Manifestations, and Management1
John F. Bruzzi, FFRRCSI,
Ritsuko Komaki, MD,
Garrett L. Walsh, MD,
Mylene T. Truong, MD,
Gregory W. Gladish, MD,
Reginald F. Munden, MD, and
Jeremy J. Erasmus, MD
1 From the Division of Diagnostic Imaging (J.F.B., M.T.T., G.W.G., R.F.M., J.J.E.), Department of Radiation Oncology (R.K.), and Department of Thoracic and Cardiovascular Surgery (G.L.W.), M. D. Anderson Cancer Center, Houston, Tex. Received March 9, 2007; revision requested May 25 and received June 26; accepted June 29. All authors have no financial relationships to disclose.
Address correspondence to J.F.B., Department of Radiology, University College Hospital Galway, Galway, Ireland (e-mail: John.Bruzzi{at}hse.ie).
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Abstract
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Non–small cell carcinomas of the superior pulmonary sulcus represent 3% of all lung cancers and are associated in most cases with a poor clinical outcome. Multimodality therapy with irradiation, chemotherapy, and surgery offers the best possibility for long-term survival and cure in most cases. For patients with pulmonary sulcus tumors that are not surgically resectable, chemoradiotherapy may help prolong survival and provide long-term pain relief. To accurately determine tumor resectability and to help optimize the planning and delivery of therapy, radiologists need a detailed knowledge of the clinical and imaging manifestations of disease in the individual patient and an awareness of the therapeutic options available. Accurate three-dimensional imaging and image interpretation are essential for mapping of the primary tumor before irradiation or surgical resection. Familiarity with the complex anatomy of the superior pulmonary sulcus is particularly crucial for determining the local-regional extension of a tumor and the most appropriate surgical approach.
© RSNA, 2008
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LEARNING OBJECTIVES FOR TEST 5
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After reading this article and taking the test, the reader will be able to:
- Identify the three compartments of the superior sulcus and their contents.
- Describe the relations between the clinical manifestations of a superior sulcus tumor and the anatomic structures involved.
- Discuss how the imaging characteristics of a superior sulcus tumor may affect disease management.
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Introduction
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In 1924, Pancoast published an article about four patients with shoulder and arm pain, atrophy of the intrinsic muscles of the hand, and ipsilateral Horner syndrome associated with a tumor arising from the apex of the lung (1). Pancoast believed that the tumors derived from epithelial rests of the fifth branchial cleft; however, their bronchopulmonary origin was later correctly recognized by Tobias (2). Strictly defined, Pancoast tumors are non–small cell carcinomas that originate in the lung apex and that often cause signs and symptoms known collectively as Pancoast syndrome. These manifestations may include pain in the shoulder girdle and arm, as well as Horner syndrome, which is characterized by ipsilateral anhidrosis of the face, miosis, and ptosis with narrowing of the palpebral fissure secondary to paralysis of the Müller muscle. (The muscle paralysis results from invasion of the cervical sympathetic ganglion.) Because not all tumors of the lung apex cause Pancoast syndrome, 
the term superior pulmonary sulcus tumor is usually used in clinical practice to describe all non–small cell carcinomas that arise from the lung apex and invade the chest wall or the soft tissues of the thoracic inlet, regardless of the complex of symptoms.
In patients with a potentially resectable tumor, multimodality treatment in which surgery is combined with pre- or postoperative radiation therapy, with or without chemotherapy, now forms the standard of care for patients with superior sulcus tumors. Optimal management of these tumors requires knowledge of the different therapeutic options available and an understanding of . how the complex anatomy of the superior sulcus and local extension of the tumor affect resectability This article describes the anatomy, clinical manifestations, and current management options available to patients with a superior pulmonary . sulcus tumor. The multidisciplinary approach for achieving optimal management is explained indetail
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Anatomy of the Superior Sulcus
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In the context of surgical management, it is useful to conceptualize the anatomy of the superior sulcus as being divided into anterior, middle, and posterior compartments by the scalene muscles (3) (Fig 1). The anterior compartment contains the subclavian vein; the middle compartment (interscalene triangle) contains the subclavian artery and its branches, as well as the trunks of the brachial plexus; and the posterior compartment contains the costovertebral groove, the roots of the brachial plexus, and the stellate ganglion.
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Figure 1. Three-dimensional drawing shows the surgical anatomy of the superior sulcus. The superior sulcus is divided into anterior, middle, and posterior compartments by the scalene muscles. The anterior scalene muscle extends obliquely, inferiorly, and laterally from the anterior tubercles of the transverse processes of C3 through C6 to the site of its insertion on the anterolateral portion of the first rib. The middle-posterior scalene muscle complex extends from the posterior tubercles of the transverse processes of C2 through C7 to insert more laterally on the first and second ribs, dividing the superior sulcus into three compartments. On the right, the anterior scalene muscle has been partially removed to show the components of the middle compartment. The arrow indicates the stellate ganglion. L = lower trunk of brachial plexus, M = middle trunk of brachial plexus, SA = subclavian artery, SV = subclavian vein, U = upper trunk of brachial plexus.
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On radiologic images, particularly on images obtained in the most medial, juxtamediastinal portion of the superior sulcus, it may be difficult to distinguish these compartments. However, it is important to be able to relate the radiologic features of the anatomy to surgical landmarks when planning the surgical approach. Sagittal T1-weighted magnetic resonance (MR) images provide most of the necessary diagnostic information and optimally depict the scalene muscles, the components of the brachial plexus and the subclavian vessels, and the apical pleura in cross sections (Fig 2). On the first few medial sagittal images, the posterior compartment of the superior sulcus is in continuity with the middle and anterior compartments below the cervical insertions of the scalene muscles; it is bounded posteriorly by the head of the first rib and anteriorly by the posterior aspect of the vertebral artery. The subclavian artery is well visualized in the middle compartment, where it originates from the aorta or brachiocephalic artery. The subclavian vein is found in the anterior compartment, where it joins with the internal jugular vein to form the brachiocephalic vein.
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Figure 2a. Normal and abnormal radiologic anatomy of the brachial plexus. (a) Sagittal T1-weighted MR image of the superior sulcus shows the courses of the C5 through T1 nerve roots laterally and inferiorly from the neurovertebral foramina. The T1 nerve root is located inferior to the neck of the first rib (R). (b) Sagittal T1-weighted MR image at the level of the interscalene space shows the anterior (AS) and posterior (PS) scalene muscles and the subclavian artery (*), which courses between them. The lower (L), middle (M) and upper (U) trunks of the brachial plexus also are visible, and the dorsal scapular artery (arrowhead) is visible between the middle and lower trunks of the brachial plexus. A superior sulcus tumor (SST) is invading the second and third ribs. V = subclavian vein, R = neck of the first rib. (c) Sagittal T1-weighted MR image at the level of the retropectoral space shows the lateral (L), posterior (P), and medial (M) cords of the brachial plexus, named according to their relationship with the axillary artery (*). R = first rib, SA = serratus anterior muscle, SC = subclavius muscle, V = axillary vein.
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Figure 2b. Normal and abnormal radiologic anatomy of the brachial plexus. (a) Sagittal T1-weighted MR image of the superior sulcus shows the courses of the C5 through T1 nerve roots laterally and inferiorly from the neurovertebral foramina. The T1 nerve root is located inferior to the neck of the first rib (R). (b) Sagittal T1-weighted MR image at the level of the interscalene space shows the anterior (AS) and posterior (PS) scalene muscles and the subclavian artery (*), which courses between them. The lower (L), middle (M) and upper (U) trunks of the brachial plexus also are visible, and the dorsal scapular artery (arrowhead) is visible between the middle and lower trunks of the brachial plexus. A superior sulcus tumor (SST) is invading the second and third ribs. V = subclavian vein, R = neck of the first rib. (c) Sagittal T1-weighted MR image at the level of the retropectoral space shows the lateral (L), posterior (P), and medial (M) cords of the brachial plexus, named according to their relationship with the axillary artery (*). R = first rib, SA = serratus anterior muscle, SC = subclavius muscle, V = axillary vein.
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Figure 2c. Normal and abnormal radiologic anatomy of the brachial plexus. (a) Sagittal T1-weighted MR image of the superior sulcus shows the courses of the C5 through T1 nerve roots laterally and inferiorly from the neurovertebral foramina. The T1 nerve root is located inferior to the neck of the first rib (R). (b) Sagittal T1-weighted MR image at the level of the interscalene space shows the anterior (AS) and posterior (PS) scalene muscles and the subclavian artery (*), which courses between them. The lower (L), middle (M) and upper (U) trunks of the brachial plexus also are visible, and the dorsal scapular artery (arrowhead) is visible between the middle and lower trunks of the brachial plexus. A superior sulcus tumor (SST) is invading the second and third ribs. V = subclavian vein, R = neck of the first rib. (c) Sagittal T1-weighted MR image at the level of the retropectoral space shows the lateral (L), posterior (P), and medial (M) cords of the brachial plexus, named according to their relationship with the axillary artery (*). R = first rib, SA = serratus anterior muscle, SC = subclavius muscle, V = axillary vein.
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On sagittal images obtained in a more lateral position, the roots of the brachial plexus can be identified as they emerge from the neurovertebral foramina. The T1 nerve root runs below the head and neck of the first rib. The C8 nerve root, which is located just above the first rib (Fig 2a), merges laterally with the T1 nerve root to form the lower trunk of the brachial plexus (Fig 2b). From their sites of origin above the C8 and T1 nerve roots, the C5 through C7 nerve roots course downward and laterally. The sympathetic stellate ganglion, which is situated immediately anterior to the head of the first rib and the transverse process of the seventh cervical vertebra, is not easily identifiable on sagittal images. On axial T1-weighted MR images, its position is predictable on the basis of the location of the head of the first rib.
In more lateral sagittal sections, the superior sulcus is more clearly divided by the scalene muscles into anterior, middle (interscalene), and posterior compartments (Fig 2b). The subclavian vein is anterior to the anterior scalene muscle. The interscalene compartment contains, from the most superior to the most inferior level, the trunks of the brachial plexus (superior, middle, and inferior), the subclavian artery, the Sibson fascia, and the apical pleura. The dorsal scapular artery is seen in most cases as a tiny flow void superior to the subclavian artery and between the inferior and middle trunks of the brachial plexus. A thin sliver of fat normally separates the apical pleura from the T1 nerve root medially and the subclavian artery laterally. Obliteration of this fat plane typically signifies tumor invasion of the soft tissues of the superior sulcus and the possibility of tumor involvement of the T1 nerve root and subclavian artery. However, because the brachial plexus is surrounded by a connective-tissue sheath, a tumor may indent the brachial plexus and displace the nerve roots or trunks superiorly without actually invading them. Sensory dysfunction may occur merely because of extrinsic nerve compression, whereas a loss of motor function is more likely to be indicative of frank invasion of the nerve. To avoid overestimating brachial plexus involvement when evaluating the local extension of a tumor, it is important to correlate the imaging findings with the patient’s symptoms.
Lateral to the costal insertion sites of the scalene muscles, the subclavian vessels pass over the first rib and enter the retropectoral space to become the axillary vessels. The trunks of the brachial plexus divide as they exit the interscalene compartment and then re-form at a location superior to the axillary artery as the lateral, posterior, and medial cords of the brachial plexus. The cords are named with respect to their relationship to the axillary artery; however, in sagittal cross section, the lateral cord is located anteriorly, the medial cord is located posteriorly, and the posterior cord is located superiorly (Fig 2c).
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Clinical Manifestations
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Superior sulcus tumors represent approximately 3% of primary non–small cell lung carcinomas (4). Adenocarcinomas have accounted for most such tumors in recent series (4–7), although in earlier reports squamous cell carcinomas were predominant (8,9). Because of the peripheral location of such lesions in the lung apex, the usual symptoms of lung cancer (eg, cough, dyspnea, and hemoptysis) are generally absent. Typically, patients present with pain confined to the shoulder or radiating to the arm, and they may undergo erroneous treatment for bursitis, osteoarthritis, or ulnar nerve entrapment before the correct diagnosis is made.
Classic Pancoast tumors arise from the lung apex, invade the costovertebral groove in the posterior compartment of the superior sulcus, and are associated with the Pancoast syndrome. Tumors in this location usually also invade the parietal pleura, causing nonspecific shoulder pain that typically radiates down the medial aspect of the scapula. They often involve the T1 nerve root, causing pain that radiates along the medial aspect of the arm and forearm as far as the wrist, and may invade the stellate ganglion (lower cervicothoracic sympathetic nerve plexus), causing the typical manifestations of Horner syndrome, which include ptosis (narrowing of the palpebral fissure), miosis (pupillary constriction), and anhidrosis (absence of sweating on one side of the face). Such tumors also typically invade the first, second, and third ribs posteriorly. Superior extension of a Pancoast tumor may result in encasement of the C8 nerve root, with resultant pain in the medial two digits of the hand and atrophy of the intrinsic muscles of the hand. Anterior extension into the tracheoesophageal groove may result in vagal or recurrent laryngeal nerve palsy (10) (Fig 3). Superomedial extension may result in involvement of the vertebral artery, vertebral bodies, neurovertebral foramina, and spinal canal, with a consequent risk of paraplegia.
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Figure 3a. Superior sulcus tumor in a 56-year-old man with sensory loss in the region of the left ulnar nerve distribution and with hoarseness. (a) Axial computed tomographic (CT) image shows a soft-tissue mass (SST) in the left lung apex, with destruction of the first and second ribs. The tumor abuts the left subclavian artery anteriorly (arrow) and has invaded the T2 vertebral body (V) medially. There is also extension of the tumor into the T2–3 neurovertebral foramen (arrowhead). T = trachea. (b) Axial MR image at the same level as a clearly shows the mass (SST) invading the T2–3 neurovertebral foramen (arrowheads) and compressing the left subclavian artery (arrow). T = trachea, V = T2 vertebral body. (c) Sagittal MR image at the level of the left superior sulcus shows the mass (SST) invading the fat above the apical pleura and encasing the subclavian artery (*). The upper (U) and middle (M) trunks of the brachial plexus are clearly separate from the mass, but the lower trunk has been encased and is no longer visible, which means that the tumor is not resectable. The tumor also has invaded the first rib (R). (d) Coronal maximum intensity projection image from hybrid positron emission tomography (PET)/CT shows intense uptake of fluorine 18 fluorodeoxyglucose (FDG) in the left superior sulcus tumor (SST) and asymmetric FDG uptake in the right vocal cord (arrow) and in the region of the right adrenal gland (arrowhead). (e) Axial fused PET/CT image at the level of the vocal cords shows increased FDG uptake by the arytenoid insertion of the right vocal cord (arrow). Because of paralysis secondary to vagal nerve palsy from the mass in the left superior sulcus, the left vocal cord is not FDG avid. (f) Axial fused PET/CT image at the level of the adrenal glands shows an FDG-avid right adrenal nodule (arrowhead) that was found at subsequent biopsy to be an adrenal metastasis.
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Figure 3b. Superior sulcus tumor in a 56-year-old man with sensory loss in the region of the left ulnar nerve distribution and with hoarseness. (a) Axial computed tomographic (CT) image shows a soft-tissue mass (SST) in the left lung apex, with destruction of the first and second ribs. The tumor abuts the left subclavian artery anteriorly (arrow) and has invaded the T2 vertebral body (V) medially. There is also extension of the tumor into the T2–3 neurovertebral foramen (arrowhead). T = trachea. (b) Axial MR image at the same level as a clearly shows the mass (SST) invading the T2–3 neurovertebral foramen (arrowheads) and compressing the left subclavian artery (arrow). T = trachea, V = T2 vertebral body. (c) Sagittal MR image at the level of the left superior sulcus shows the mass (SST) invading the fat above the apical pleura and encasing the subclavian artery (*). The upper (U) and middle (M) trunks of the brachial plexus are clearly separate from the mass, but the lower trunk has been encased and is no longer visible, which means that the tumor is not resectable. The tumor also has invaded the first rib (R). (d) Coronal maximum intensity projection image from hybrid positron emission tomography (PET)/CT shows intense uptake of fluorine 18 fluorodeoxyglucose (FDG) in the left superior sulcus tumor (SST) and asymmetric FDG uptake in the right vocal cord (arrow) and in the region of the right adrenal gland (arrowhead). (e) Axial fused PET/CT image at the level of the vocal cords shows increased FDG uptake by the arytenoid insertion of the right vocal cord (arrow). Because of paralysis secondary to vagal nerve palsy from the mass in the left superior sulcus, the left vocal cord is not FDG avid. (f) Axial fused PET/CT image at the level of the adrenal glands shows an FDG-avid right adrenal nodule (arrowhead) that was found at subsequent biopsy to be an adrenal metastasis.
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Figure 3c. Superior sulcus tumor in a 56-year-old man with sensory loss in the region of the left ulnar nerve distribution and with hoarseness. (a) Axial computed tomographic (CT) image shows a soft-tissue mass (SST) in the left lung apex, with destruction of the first and second ribs. The tumor abuts the left subclavian artery anteriorly (arrow) and has invaded the T2 vertebral body (V) medially. There is also extension of the tumor into the T2–3 neurovertebral foramen (arrowhead). T = trachea. (b) Axial MR image at the same level as a clearly shows the mass (SST) invading the T2–3 neurovertebral foramen (arrowheads) and compressing the left subclavian artery (arrow). T = trachea, V = T2 vertebral body. (c) Sagittal MR image at the level of the left superior sulcus shows the mass (SST) invading the fat above the apical pleura and encasing the subclavian artery (*). The upper (U) and middle (M) trunks of the brachial plexus are clearly separate from the mass, but the lower trunk has been encased and is no longer visible, which means that the tumor is not resectable. The tumor also has invaded the first rib (R). (d) Coronal maximum intensity projection image from hybrid positron emission tomography (PET)/CT shows intense uptake of fluorine 18 fluorodeoxyglucose (FDG) in the left superior sulcus tumor (SST) and asymmetric FDG uptake in the right vocal cord (arrow) and in the region of the right adrenal gland (arrowhead). (e) Axial fused PET/CT image at the level of the vocal cords shows increased FDG uptake by the arytenoid insertion of the right vocal cord (arrow). Because of paralysis secondary to vagal nerve palsy from the mass in the left superior sulcus, the left vocal cord is not FDG avid. (f) Axial fused PET/CT image at the level of the adrenal glands shows an FDG-avid right adrenal nodule (arrowhead) that was found at subsequent biopsy to be an adrenal metastasis.
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Figure 3d. Superior sulcus tumor in a 56-year-old man with sensory loss in the region of the left ulnar nerve distribution and with hoarseness. (a) Axial computed tomographic (CT) image shows a soft-tissue mass (SST) in the left lung apex, with destruction of the first and second ribs. The tumor abuts the left subclavian artery anteriorly (arrow) and has invaded the T2 vertebral body (V) medially. There is also extension of the tumor into the T2–3 neurovertebral foramen (arrowhead). T = trachea. (b) Axial MR image at the same level as a clearly shows the mass (SST) invading the T2–3 neurovertebral foramen (arrowheads) and compressing the left subclavian artery (arrow). T = trachea, V = T2 vertebral body. (c) Sagittal MR image at the level of the left superior sulcus shows the mass (SST) invading the fat above the apical pleura and encasing the subclavian artery (*). The upper (U) and middle (M) trunks of the brachial plexus are clearly separate from the mass, but the lower trunk has been encased and is no longer visible, which means that the tumor is not resectable. The tumor also has invaded the first rib (R). (d) Coronal maximum intensity projection image from hybrid positron emission tomography (PET)/CT shows intense uptake of fluorine 18 fluorodeoxyglucose (FDG) in the left superior sulcus tumor (SST) and asymmetric FDG uptake in the right vocal cord (arrow) and in the region of the right adrenal gland (arrowhead). (e) Axial fused PET/CT image at the level of the vocal cords shows increased FDG uptake by the arytenoid insertion of the right vocal cord (arrow). Because of paralysis secondary to vagal nerve palsy from the mass in the left superior sulcus, the left vocal cord is not FDG avid. (f) Axial fused PET/CT image at the level of the adrenal glands shows an FDG-avid right adrenal nodule (arrowhead) that was found at subsequent biopsy to be an adrenal metastasis.
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Figure 3e. Superior sulcus tumor in a 56-year-old man with sensory loss in the region of the left ulnar nerve distribution and with hoarseness. (a) Axial computed tomographic (CT) image shows a soft-tissue mass (SST) in the left lung apex, with destruction of the first and second ribs. The tumor abuts the left subclavian artery anteriorly (arrow) and has invaded the T2 vertebral body (V) medially. There is also extension of the tumor into the T2–3 neurovertebral foramen (arrowhead). T = trachea. (b) Axial MR image at the same level as a clearly shows the mass (SST) invading the T2–3 neurovertebral foramen (arrowheads) and compressing the left subclavian artery (arrow). T = trachea, V = T2 vertebral body. (c) Sagittal MR image at the level of the left superior sulcus shows the mass (SST) invading the fat above the apical pleura and encasing the subclavian artery (*). The upper (U) and middle (M) trunks of the brachial plexus are clearly separate from the mass, but the lower trunk has been encased and is no longer visible, which means that the tumor is not resectable. The tumor also has invaded the first rib (R). (d) Coronal maximum intensity projection image from hybrid positron emission tomography (PET)/CT shows intense uptake of fluorine 18 fluorodeoxyglucose (FDG) in the left superior sulcus tumor (SST) and asymmetric FDG uptake in the right vocal cord (arrow) and in the region of the right adrenal gland (arrowhead). (e) Axial fused PET/CT image at the level of the vocal cords shows increased FDG uptake by the arytenoid insertion of the right vocal cord (arrow). Because of paralysis secondary to vagal nerve palsy from the mass in the left superior sulcus, the left vocal cord is not FDG avid. (f) Axial fused PET/CT image at the level of the adrenal glands shows an FDG-avid right adrenal nodule (arrowhead) that was found at subsequent biopsy to be an adrenal metastasis.
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Figure 3f. Superior sulcus tumor in a 56-year-old man with sensory loss in the region of the left ulnar nerve distribution and with hoarseness. (a) Axial computed tomographic (CT) image shows a soft-tissue mass (SST) in the left lung apex, with destruction of the first and second ribs. The tumor abuts the left subclavian artery anteriorly (arrow) and has invaded the T2 vertebral body (V) medially. There is also extension of the tumor into the T2–3 neurovertebral foramen (arrowhead). T = trachea. (b) Axial MR image at the same level as a clearly shows the mass (SST) invading the T2–3 neurovertebral foramen (arrowheads) and compressing the left subclavian artery (arrow). T = trachea, V = T2 vertebral body. (c) Sagittal MR image at the level of the left superior sulcus shows the mass (SST) invading the fat above the apical pleura and encasing the subclavian artery (*). The upper (U) and middle (M) trunks of the brachial plexus are clearly separate from the mass, but the lower trunk has been encased and is no longer visible, which means that the tumor is not resectable. The tumor also has invaded the first rib (R). (d) Coronal maximum intensity projection image from hybrid positron emission tomography (PET)/CT shows intense uptake of fluorine 18 fluorodeoxyglucose (FDG) in the left superior sulcus tumor (SST) and asymmetric FDG uptake in the right vocal cord (arrow) and in the region of the right adrenal gland (arrowhead). (e) Axial fused PET/CT image at the level of the vocal cords shows increased FDG uptake by the arytenoid insertion of the right vocal cord (arrow). Because of paralysis secondary to vagal nerve palsy from the mass in the left superior sulcus, the left vocal cord is not FDG avid. (f) Axial fused PET/CT image at the level of the adrenal glands shows an FDG-avid right adrenal nodule (arrowhead) that was found at subsequent biopsy to be an adrenal metastasis.
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Tumors with a lateral location that invade the interscalene triangle (middle compartment) of the superior sulcus may encase the subclavian artery and involve the trunks of the brachial plexus (Fig 3). The symptoms that result from brachial plexus involvement are similar to those caused by a classic Pancoast tumor but may not include Horner syndrome unless posteromedial tumor extension results in involvement of the stellate ganglion.
The anterior compartment of the superior sulcus contains the subclavian vein and the costoclavicular space. The phrenic nerve runs caudad on the anterior aspect of the anterior scalene muscle. Tumor invasion in this compartment may cause signs and symptoms of venous obstruction and ipsilateral diaphragmatic paralysis; however, brachial plexus involvement occurs only if the tumor also extends into the interscalene triangle (the middle compartment). Tumors located more laterally in the superior sulcus may invade the subclavian vessels and cords of the brachial plexus where those structures pass over the first rib into the retropectoral space (Fig 4). Such tumors are not commonly associated with Horner syndrome unless they are advanced and have extended as far medially as the mediastinum.
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Figure 4a. Superior sulcus tumor in an 84-year-old man with a 3-month history of shoulder pain and atrophy of the intrinsic muscles of the hand. (a) Frontal chest radiograph shows a large spiculated mass in the lateral portion of the right lung apex, with associated rib destruction. (b) Axial CT image at the level of the thoracic inlet shows the soft-tissue mass (SST) extending laterally into the costoclavicular space (arrow) and eroding the first and second ribs. (c, d) Sagittal T1-weighted MR images of the lateral portion of the superior sulcus before (c) and after (d) gadolinium administration show the necrotic tumor (SST) with destruction of the first rib, encasement of the medial cord of the brachial plexus (arrow), and partial adherence of the tumor to the subclavian artery (*). The clinical and radiologic manifestations were diagnostic of advanced-stage (T4) local-regional disease precluding curative surgical resection. The patient underwent definitive radiation therapy. C = clavicle, V = subclavian vein.
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Figure 4b. Superior sulcus tumor in an 84-year-old man with a 3-month history of shoulder pain and atrophy of the intrinsic muscles of the hand. (a) Frontal chest radiograph shows a large spiculated mass in the lateral portion of the right lung apex, with associated rib destruction. (b) Axial CT image at the level of the thoracic inlet shows the soft-tissue mass (SST) extending laterally into the costoclavicular space (arrow) and eroding the first and second ribs. (c, d) Sagittal T1-weighted MR images of the lateral portion of the superior sulcus before (c) and after (d) gadolinium administration show the necrotic tumor (SST) with destruction of the first rib, encasement of the medial cord of the brachial plexus (arrow), and partial adherence of the tumor to the subclavian artery (*). The clinical and radiologic manifestations were diagnostic of advanced-stage (T4) local-regional disease precluding curative surgical resection. The patient underwent definitive radiation therapy. C = clavicle, V = subclavian vein.
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Figure 4c. Superior sulcus tumor in an 84-year-old man with a 3-month history of shoulder pain and atrophy of the intrinsic muscles of the hand. (a) Frontal chest radiograph shows a large spiculated mass in the lateral portion of the right lung apex, with associated rib destruction. (b) Axial CT image at the level of the thoracic inlet shows the soft-tissue mass (SST) extending laterally into the costoclavicular space (arrow) and eroding the first and second ribs. (c, d) Sagittal T1-weighted MR images of the lateral portion of the superior sulcus before (c) and after (d) gadolinium administration show the necrotic tumor (SST) with destruction of the first rib, encasement of the medial cord of the brachial plexus (arrow), and partial adherence of the tumor to the subclavian artery (*). The clinical and radiologic manifestations were diagnostic of advanced-stage (T4) local-regional disease precluding curative surgical resection. The patient underwent definitive radiation therapy. C = clavicle, V = subclavian vein.
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Figure 4d. Superior sulcus tumor in an 84-year-old man with a 3-month history of shoulder pain and atrophy of the intrinsic muscles of the hand. (a) Frontal chest radiograph shows a large spiculated mass in the lateral portion of the right lung apex, with associated rib destruction. (b) Axial CT image at the level of the thoracic inlet shows the soft-tissue mass (SST) extending laterally into the costoclavicular space (arrow) and eroding the first and second ribs. (c, d) Sagittal T1-weighted MR images of the lateral portion of the superior sulcus before (c) and after (d) gadolinium administration show the necrotic tumor (SST) with destruction of the first rib, encasement of the medial cord of the brachial plexus (arrow), and partial adherence of the tumor to the subclavian artery (*). The clinical and radiologic manifestations were diagnostic of advanced-stage (T4) local-regional disease precluding curative surgical resection. The patient underwent definitive radiation therapy. C = clavicle, V = subclavian vein.
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In summary, knowledge of the patient’s symptoms and any neurologic manifestations detected during the physical examination may help improve the accuracy of image interpretation. Such information may be particularly helpful in determining the local-regional extension of a tumor, a key factor when formulating the most appropriate treatment plan. For instance, tumor invasion of the brachial plexus roots or trunks above the level of the T1 nerve root is an absolute contraindication to surgery. If a patient reports pain in the medial two digits of the hand, the images from that patient should be carefully assessed for evidence of superior extension of the tumor and involvement of the C8 nerve root.
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Management Methods
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Multimodality Treatment
Superior sulcus tumors were once thought to be incurable. However, published reports by Chardack and MacCallum (11) and, later, by Shaw et al (12) about the successful resection of such tumors after radiation therapy indicated that aggressive local management could result in prolonged survival and cure. Subsequently, the results of numerous prospective and retrospective studies showed the achievement of 5-year survival rates of 26%–47% after multimodality treatment consisting of surgery and pre- or postoperative radiation therapy (4,5,7,13–16). Furthermore, the combined use of chemotherapy and radiation therapy in addition to complete surgical resection was associated with further prolongation of survival (17–20). In the largest prospective trial to date, the Southwest Oncology Group studied the utility of combined chemotherapy and radiation therapy in 110 patients with potentially resectable superior sulcus tumors (T3 or T4, N0 or N1). They demonstrated a 5-year survival of 44% for all patients who underwent combined therapy and 54% for those who subsequently underwent a complete tumor resection (median survival for the two groups was 33 months and 94 months, respectively), an improvement compared with the survival rates for historical controls (21).
Multimodality therapy with or without chemotherapy is now the standard of care for patients with superior sulcus tumors. Induction chemotherapy alone is less effective than combined chemoradiotherapy in relieving pain, an important objective of neoadjuvant therapy for superior sulcus tumors. The other aims of neoadjuvant radiation therapy and concurrent chemotherapy are to achieve control of the primary tumor and of local-regional lymphatic extension and to lower the stage of locally advanced tumors, thereby improving the chances of a complete R0 resection and reducing the risk of a local-regional recurrence. In the Southwest Oncology Group trial, patients who experienced a pathologically proved complete response to induction therapy (including 29% of the patients who underwent resection) had the best clinical outcome. Patients with residual disease after induction therapy also had improved survival (median, 30 months) compared with that for historical controls and had a lower risk of local-regional recurrence, which may cause debilitating pain (21). However, either because of interval tumor progression or because of comorbidity resulting from induction therapy, some patients who undergo multimodality therapy are not subsequently eligible for surgery. For this reason, some centers proceed directly to surgery rather than delay the potentially curative procedure, and they reserve chemotherapy and radiation therapy for adjuvant use in patients who are at high risk for recurrent or metastatic disease.
Regardless of the order in which therapies are administered, the appropriate selection of patients for surgery is essential. Komaki et al, after a retrospective study of 143 patients who underwent combined-modality treatment for superior sulcus tumors, identified a number of indicators of increased long-term (
5 years) survival. These included a lower cancer stage at presentation (5-year survival was 47% among patients with stage IIB disease vs 14% among those with stage IIIA disease and 16% among those with stage IIIB disease; P < .01), weight loss of less than 5% body weight before treatment, and surgical resection (7). However, they found that surgical resection was associated with improved survival only in the absence of nodal metastases (stage IIB) (P < .01). On the basis of this result, they concluded that surgical resection of superior sulcus tumors should not be considered in patients with mediastinal or contralateral supraclavicular nodal metastases. Accordingly, the importance of imaging for the detection of nodal metastases before the administration of treatment (eg, during mediastinoscopy or endobronchial ultrasonographically guided biopsy) cannot be overemphasized.
Radiation Therapy
When planning radiation therapy for a superior sulcus tumor, the most important factors are the potential resectability of the primary tumor, its location, and its proximity to adjacent structures such as the esophagus, brachial plexus, and spinal cord. In patients undergoing multimodality therapy for a potentially resectable superior sulcus tumor, external-beam radiation therapy with a dose of 30–45 Gy is commonly administered to the primary tumor and the surrounding tissue in the ipsilateral supraclavicular region but not to the mediastinum or hilum. After subsequent surgical resection and pathologic analysis, patients with positive tumor margins or with N2 disease confirmed at microscopy should receive postoperative radiation therapy with or without concurrent chemotherapy (3). However, in patients with disease that does not respond to preoperative low-dose radiation therapy, the proliferating clonogenic cells will be even more resistant to radiation and chemotherapy after a break of several weeks, and no additional effective treatment can be given if the tumor is not resectable (3). Determining the resectability of a superior sulcus tumor is therefore a critically important goal at baseline imaging.
Newer approaches such as intensity-modulated radiation therapy, three-dimensional conformal techniques, proton therapy, and high-energy (eg, 6 million V) external-beam radiation therapy have made it possible to deliver a dose as high as 70 Gy for definitive local control of an unresectable tumor (22). Irradiation with a smaller dose fraction of 1.2 Gy administered twice daily (for a total tumor dose of 69.6 Gy over 7 weeks) to avoid brachial plexus injury, with concurrent chemotherapy, has been successful for controlling some unresectable superior sulcus tumors (23). Because of the relative immobility of tumors in the lung apex, radiation therapy can be administered effectively, with minimal toxicity to surrounding normal tissues such as the spinal cord and the mediastinum, by using such techniques (3,24). However, to achieve local-regional control with this sort of radiation therapy regimen, the target for irradiation has to be precisely mapped; the success of therapy therefore depends on the accuracy of tumor depiction at cross-sectional imaging. CT, MR imaging, and PET are essential for obtaining accurate delineation of the gross tumor volume when planning radiation treatment (Fig 5).
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Figure 5a. Coronal (a) and sagittal (b) CT images, obtained at the level of the left superior sulcus for planning of intensity-modulated radiation treatment of an unresectable superior sulcus tumor, show the curve that will result in the delivery of a radiation dose of 66 Gy to the planned target volume. The use of intensity-modulated radiation therapy allows the targeted delivery of a dose of as much as 70 Gy with minimal toxic effects on the surrounding anatomy. Knowledge of the radiation treatment plan is useful when interpreting follow-up images.
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Figure 5b. Coronal (a) and sagittal (b) CT images, obtained at the level of the left superior sulcus for planning of intensity-modulated radiation treatment of an unresectable superior sulcus tumor, show the curve that will result in the delivery of a radiation dose of 66 Gy to the planned target volume. The use of intensity-modulated radiation therapy allows the targeted delivery of a dose of as much as 70 Gy with minimal toxic effects on the surrounding anatomy. Knowledge of the radiation treatment plan is useful when interpreting follow-up images.
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Surgery
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Surgical resection of a superior sulcus tumor is most commonly performed via a posterolateral thoracotomy, also known as the Shaw-Paulson approach (12). This approach requires an incision that extends inferiorly between the posterior spinous processes and the medial aspect of the scapula and then laterally to a point approximately 2 cm below and lateral to the angle of the scapula. This method allows the en bloc resection of a posteriorly located tumor and the involved portion of the chest wall as well as a pulmonary lobar resection or pneumonectomy. A complete resection requires the removal of all ribs that have been invaded by the tumor and of one uninvolved rib below the inferior margin of the tumor. CT and MR imaging are useful for planning the extent of the chest wall resection. Although a posterolateral thoracotomy allows the resection of posteriorly located tumors that have not invaded the thoracic inlet structures, it provides only limited access to the middle and anterior compartments of the thoracic inlet, making it more difficult to safely excise a tumor that has involved the trunks of the brachial plexus or the subclavian vessels.
An alternative approach involves the creation of an L-shaped incision in the anterior chest wall. The first leg of the L proceeds downward from the midcervical level, anterior and parallel to the sternocleidomastoid muscle. The second leg extends laterally, parallel to the clavicle in the intercostal space below the first uninvolved rib. The ribs above this level are excised, along with the involved portion of the chest wall and the medial portion of the clavicle (25,26). The anterior approach allows greater access to the subclavian vessels and brachial plexus and easier clearance of supraclavicular lymph nodes; however, pulmonary lobectomy or pneumonectomy through the resultant chest wall defect may be technically more challenging. In addition, resection of the medial portion of the clavicle may result in glenohumeral instability and functional discomfort (27). Alternative approaches in which the sternoclavicular joint is preserved include the transmanubrial approach (extended cervico-sterno-thoracotomy) (25,26) and the hemi-clamshell approach (28). The combined use of both an anterior and a posterolateral approach has been associated with a higher mortality than the use of either approach alone (29).
Imaging plays a vital role in selecting the most appropriate surgical approach. It helps determine the exact location of the primary tumor, its relations with surrounding anatomic structures, and its resectability. Posteriorly located tumors are amenable to resection through a posterolateral incision, but tumors that involve the trunks of the brachial plexus or the subclavian vessels usually require an anterior approach.
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Summary
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Combined-modality therapy is the standard of care for patients with superior sulcus tumors. For optimal planning and effective administration of such therapy, accurate imaging and image interpretation are essential. Image interpretation is facilitated by a familiarity with the anatomy of the superior sulcus; an understanding of the importance of accurate delineation of local-regional disease and detection of nodal metastases; and knowledge of the specific clinical manifestations in each patient.
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Acknowledgments
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We thank David Bier for the use of his drawing of the surgical anatomy of the superior sulcus.
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Footnotes
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Abbreviations: FDG = fluorodeoxyglucose
See also the article by Bruzzi et al (pp 561–572) in this issue.
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References
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Related Article
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Imaging of Non–Small Cell Lung Cancer of the Superior Sulcus: Part 2: Initial Staging and Assessment of Resectability and Therapeutic Response
- John F. Bruzzi, Ritsuko Komaki, Garrett L. Walsh, Mylene T. Truong, Gregory W. Gladish, Reginald F. Munden, and Jeremy J. Erasmus
RadioGraphics 2008 28: 561-572.
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Abstract
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