DOI: 10.1148/rg.282075710
RadioGraphics 2008;28:561-572
© RSNA, 2008
Imaging of Non–Small Cell Lung Cancer of the Superior Sulcus
Part 2: Initial Staging and Assessment of Resectability and Therapeutic Response1
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; 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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Imaging plays a crucial role in the diagnosis and staging of superior sulcus tumors, assessment of their resectability, determination of the optimal approach to disease management, and evaluation of the response to therapy. Computed tomography (CT), magnetic resonance (MR) imaging, and positron emission tomography (PET)/CT contribute important and complementary information. Whereas CT is optimal for depicting bone erosion and for staging of intrathoracic disease, MR imaging is superior for evaluating tumor extension to the intervertebral neural foramina, the spinal cord, and the brachial plexus, primarily because of the higher contrast resolution and multiplanar capability available with MR imaging technology. Use of PET/CT enables the detection of unsuspected nodal and distant metastases. However, imaging has only limited usefulness for evaluating the response of a tumor to induction therapy and detecting local recurrence, and surgical biopsy often is necessary to verify the results of therapy.
© RSNA, 2008
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Introduction
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Imaging is important for establishing the location and anatomic extension of a superior sulcus tumor and, thus, the most appropriate treatment. Imaging in patients with superior sulcus tumors is directed toward optimal TNM classification of the tumor and identification of local and regional factors that may influence the type of treatment prescribed. This article describes the role of imaging in the initial clinical staging of superior sulcus tumors as well as in the assessment of tumor resectability and response to therapy.
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Staging
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Superior sulcus tumors are staged according to the standard American Joint Commission on Cancer (AJCC) guidelines for staging of non–small cell lung cancer (1). By definition, superior sulcus tumors are classified as stage IIB (T3 N0) or higher because they invade extrathoracic soft tissues. However, neither involvement of the brachial plexus nor involvement of the subclavian vessels is defined in the standard AJCC staging system for lung cancer. 
Limited involvement of the lower trunk or roots of the brachial plexus (C8 and T1 nerves) is generally regarded as T3 disease (Fig 1), whereas more extensive invasion of the brachial plexus trunks or roots (C5 through C7 nerves), subclavian vessels, vertebral bodies, spinal cord, trachea, or esophagus constitutes T4 disease (Fig 2). Nevertheless, it is important to be aware that the classification of a superior sulcus lung carcinoma as T4 disease does not always imply unresectability of the tumor. It is also important to realize that invasive disease in the superior sulcus often does not respect normal anatomic boundaries and may involve any or all compartments of the superior sulcus. Therefore, in disease staging, the objective of imaging is to accurately determine the local-regional extension of the tumor and its resectability.
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Figure 1a. Superior sulcus tumor in a 59-year-old man with ptosis of the left eyelid and pain radiating from the left shoulder to the medial two digits of the left hand but without motor dysfunction. (a) Axial computed tomographic (CT) image at the apex of the thorax obtained as part of a neck CT examination shows a superior sulcus tumor (SST). The mass clearly abuts the neurovertebral foramen, but the presence and degree of any extension into the foramen are difficult to determine. T = trachea, V = vertebral body. (b) Axial T1-weighted magnetic resonance (MR) image of the left superior sulcus shows extension of the tumor (SST) posteriorly into the T1–2 neurovertebral foramen (*). Intraforaminal extension is an important finding because complete resection of the tumor in such a case requires the participation of both a thoracic surgeon and a neurosurgeon. T = trachea, V = vertebral body. (c–e) Sagittal T1-weighted MR images show tumor (SST) extension into the T1–2 neurovertebral foramen (*) and obliteration of the exiting T1 nerve root. The C8 nerve root is preserved proximally (arrowhead in c), but laterally, where the tumor abuts it (arrowhead in d), it appears thickened. In e, the lower trunk of the brachial plexus in the interscalene space appears to be totally encased, but the dorsal scapular artery (arrow), which separates the lower trunk of the brachial plexus from the middle and upper trunks, is visible just superior to the tumor. Because the patient was not experiencing any motor dysfunction, surgery was performed, and the tumor was successfully separated from the lower trunk of the brachial plexus.
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Figure 1b. Superior sulcus tumor in a 59-year-old man with ptosis of the left eyelid and pain radiating from the left shoulder to the medial two digits of the left hand but without motor dysfunction. (a) Axial computed tomographic (CT) image at the apex of the thorax obtained as part of a neck CT examination shows a superior sulcus tumor (SST). The mass clearly abuts the neurovertebral foramen, but the presence and degree of any extension into the foramen are difficult to determine. T = trachea, V = vertebral body. (b) Axial T1-weighted magnetic resonance (MR) image of the left superior sulcus shows extension of the tumor (SST) posteriorly into the T1–2 neurovertebral foramen (*). Intraforaminal extension is an important finding because complete resection of the tumor in such a case requires the participation of both a thoracic surgeon and a neurosurgeon. T = trachea, V = vertebral body. (c–e) Sagittal T1-weighted MR images show tumor (SST) extension into the T1–2 neurovertebral foramen (*) and obliteration of the exiting T1 nerve root. The C8 nerve root is preserved proximally (arrowhead in c), but laterally, where the tumor abuts it (arrowhead in d), it appears thickened. In e, the lower trunk of the brachial plexus in the interscalene space appears to be totally encased, but the dorsal scapular artery (arrow), which separates the lower trunk of the brachial plexus from the middle and upper trunks, is visible just superior to the tumor. Because the patient was not experiencing any motor dysfunction, surgery was performed, and the tumor was successfully separated from the lower trunk of the brachial plexus.
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Figure 1c. Superior sulcus tumor in a 59-year-old man with ptosis of the left eyelid and pain radiating from the left shoulder to the medial two digits of the left hand but without motor dysfunction. (a) Axial computed tomographic (CT) image at the apex of the thorax obtained as part of a neck CT examination shows a superior sulcus tumor (SST). The mass clearly abuts the neurovertebral foramen, but the presence and degree of any extension into the foramen are difficult to determine. T = trachea, V = vertebral body. (b) Axial T1-weighted magnetic resonance (MR) image of the left superior sulcus shows extension of the tumor (SST) posteriorly into the T1–2 neurovertebral foramen (*). Intraforaminal extension is an important finding because complete resection of the tumor in such a case requires the participation of both a thoracic surgeon and a neurosurgeon. T = trachea, V = vertebral body. (c–e) Sagittal T1-weighted MR images show tumor (SST) extension into the T1–2 neurovertebral foramen (*) and obliteration of the exiting T1 nerve root. The C8 nerve root is preserved proximally (arrowhead in c), but laterally, where the tumor abuts it (arrowhead in d), it appears thickened. In e, the lower trunk of the brachial plexus in the interscalene space appears to be totally encased, but the dorsal scapular artery (arrow), which separates the lower trunk of the brachial plexus from the middle and upper trunks, is visible just superior to the tumor. Because the patient was not experiencing any motor dysfunction, surgery was performed, and the tumor was successfully separated from the lower trunk of the brachial plexus.
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Figure 1d. Superior sulcus tumor in a 59-year-old man with ptosis of the left eyelid and pain radiating from the left shoulder to the medial two digits of the left hand but without motor dysfunction. (a) Axial computed tomographic (CT) image at the apex of the thorax obtained as part of a neck CT examination shows a superior sulcus tumor (SST). The mass clearly abuts the neurovertebral foramen, but the presence and degree of any extension into the foramen are difficult to determine. T = trachea, V = vertebral body. (b) Axial T1-weighted magnetic resonance (MR) image of the left superior sulcus shows extension of the tumor (SST) posteriorly into the T1–2 neurovertebral foramen (*). Intraforaminal extension is an important finding because complete resection of the tumor in such a case requires the participation of both a thoracic surgeon and a neurosurgeon. T = trachea, V = vertebral body. (c–e) Sagittal T1-weighted MR images show tumor (SST) extension into the T1–2 neurovertebral foramen (*) and obliteration of the exiting T1 nerve root. The C8 nerve root is preserved proximally (arrowhead in c), but laterally, where the tumor abuts it (arrowhead in d), it appears thickened. In e, the lower trunk of the brachial plexus in the interscalene space appears to be totally encased, but the dorsal scapular artery (arrow), which separates the lower trunk of the brachial plexus from the middle and upper trunks, is visible just superior to the tumor. Because the patient was not experiencing any motor dysfunction, surgery was performed, and the tumor was successfully separated from the lower trunk of the brachial plexus.
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Figure 1e. Superior sulcus tumor in a 59-year-old man with ptosis of the left eyelid and pain radiating from the left shoulder to the medial two digits of the left hand but without motor dysfunction. (a) Axial computed tomographic (CT) image at the apex of the thorax obtained as part of a neck CT examination shows a superior sulcus tumor (SST). The mass clearly abuts the neurovertebral foramen, but the presence and degree of any extension into the foramen are difficult to determine. T = trachea, V = vertebral body. (b) Axial T1-weighted magnetic resonance (MR) image of the left superior sulcus shows extension of the tumor (SST) posteriorly into the T1–2 neurovertebral foramen (*). Intraforaminal extension is an important finding because complete resection of the tumor in such a case requires the participation of both a thoracic surgeon and a neurosurgeon. T = trachea, V = vertebral body. (c–e) Sagittal T1-weighted MR images show tumor (SST) extension into the T1–2 neurovertebral foramen (*) and obliteration of the exiting T1 nerve root. The C8 nerve root is preserved proximally (arrowhead in c), but laterally, where the tumor abuts it (arrowhead in d), it appears thickened. In e, the lower trunk of the brachial plexus in the interscalene space appears to be totally encased, but the dorsal scapular artery (arrow), which separates the lower trunk of the brachial plexus from the middle and upper trunks, is visible just superior to the tumor. Because the patient was not experiencing any motor dysfunction, surgery was performed, and the tumor was successfully separated from the lower trunk of the brachial plexus.
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Figure 2a. Superior sulcus tumor in a 48-year-old man without neurologic signs in the left upper extremity but with left interscapular chest wall pain suggestive of T1 nerve root invasion. (a) Frontal chest radiograph shows a soft-tissue mass in the left lung apex. (b, c) Axial CT images obtained with soft-tissue (b) and bone (c) windows at the level of the thoracic inlet depict a superior sulcus tumor (SST) with focal destruction of the T2 vertebral body (arrowhead) and probable extension into the T2–3 neurovertebral foramen (arrow in b). (d) Axial T1-weighted MR image at the same level as b helps confirm that the mass (SST) has invaded the T2 vertebral body (arrowhead) and extends into the T2–3 neurovertebral foramen (arrow) as far as the extradural space. (e, f) Comparison of sagittal T1-weighted MR images at the level of the interscalene space before (e) and after (f) the intravenous administration of gadolinium shows enhancement of the mass (SST) in f. The mass encases the subclavian artery (S) and the T1 nerve root but merely abuts the C8 nerve root, and the higher nerve roots are preserved. Despite these findings of limited invasion of the vertebral body and brachial plexus, the tumor would have been eligible for surgical resection if distant metastases (not shown) had not been found.
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Figure 2b. Superior sulcus tumor in a 48-year-old man without neurologic signs in the left upper extremity but with left interscapular chest wall pain suggestive of T1 nerve root invasion. (a) Frontal chest radiograph shows a soft-tissue mass in the left lung apex. (b, c) Axial CT images obtained with soft-tissue (b) and bone (c) windows at the level of the thoracic inlet depict a superior sulcus tumor (SST) with focal destruction of the T2 vertebral body (arrowhead) and probable extension into the T2–3 neurovertebral foramen (arrow in b). (d) Axial T1-weighted MR image at the same level as b helps confirm that the mass (SST) has invaded the T2 vertebral body (arrowhead) and extends into the T2–3 neurovertebral foramen (arrow) as far as the extradural space. (e, f) Comparison of sagittal T1-weighted MR images at the level of the interscalene space before (e) and after (f) the intravenous administration of gadolinium shows enhancement of the mass (SST) in f. The mass encases the subclavian artery (S) and the T1 nerve root but merely abuts the C8 nerve root, and the higher nerve roots are preserved. Despite these findings of limited invasion of the vertebral body and brachial plexus, the tumor would have been eligible for surgical resection if distant metastases (not shown) had not been found.
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Figure 2c. Superior sulcus tumor in a 48-year-old man without neurologic signs in the left upper extremity but with left interscapular chest wall pain suggestive of T1 nerve root invasion. (a) Frontal chest radiograph shows a soft-tissue mass in the left lung apex. (b, c) Axial CT images obtained with soft-tissue (b) and bone (c) windows at the level of the thoracic inlet depict a superior sulcus tumor (SST) with focal destruction of the T2 vertebral body (arrowhead) and probable extension into the T2–3 neurovertebral foramen (arrow in b). (d) Axial T1-weighted MR image at the same level as b helps confirm that the mass (SST) has invaded the T2 vertebral body (arrowhead) and extends into the T2–3 neurovertebral foramen (arrow) as far as the extradural space. (e, f) Comparison of sagittal T1-weighted MR images at the level of the interscalene space before (e) and after (f) the intravenous administration of gadolinium shows enhancement of the mass (SST) in f. The mass encases the subclavian artery (S) and the T1 nerve root but merely abuts the C8 nerve root, and the higher nerve roots are preserved. Despite these findings of limited invasion of the vertebral body and brachial plexus, the tumor would have been eligible for surgical resection if distant metastases (not shown) had not been found.
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Figure 2d. Superior sulcus tumor in a 48-year-old man without neurologic signs in the left upper extremity but with left interscapular chest wall pain suggestive of T1 nerve root invasion. (a) Frontal chest radiograph shows a soft-tissue mass in the left lung apex. (b, c) Axial CT images obtained with soft-tissue (b) and bone (c) windows at the level of the thoracic inlet depict a superior sulcus tumor (SST) with focal destruction of the T2 vertebral body (arrowhead) and probable extension into the T2–3 neurovertebral foramen (arrow in b). (d) Axial T1-weighted MR image at the same level as b helps confirm that the mass (SST) has invaded the T2 vertebral body (arrowhead) and extends into the T2–3 neurovertebral foramen (arrow) as far as the extradural space. (e, f) Comparison of sagittal T1-weighted MR images at the level of the interscalene space before (e) and after (f) the intravenous administration of gadolinium shows enhancement of the mass (SST) in f. The mass encases the subclavian artery (S) and the T1 nerve root but merely abuts the C8 nerve root, and the higher nerve roots are preserved. Despite these findings of limited invasion of the vertebral body and brachial plexus, the tumor would have been eligible for surgical resection if distant metastases (not shown) had not been found.
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Figure 2e. Superior sulcus tumor in a 48-year-old man without neurologic signs in the left upper extremity but with left interscapular chest wall pain suggestive of T1 nerve root invasion. (a) Frontal chest radiograph shows a soft-tissue mass in the left lung apex. (b, c) Axial CT images obtained with soft-tissue (b) and bone (c) windows at the level of the thoracic inlet depict a superior sulcus tumor (SST) with focal destruction of the T2 vertebral body (arrowhead) and probable extension into the T2–3 neurovertebral foramen (arrow in b). (d) Axial T1-weighted MR image at the same level as b helps confirm that the mass (SST) has invaded the T2 vertebral body (arrowhead) and extends into the T2–3 neurovertebral foramen (arrow) as far as the extradural space. (e, f) Comparison of sagittal T1-weighted MR images at the level of the interscalene space before (e) and after (f) the intravenous administration of gadolinium shows enhancement of the mass (SST) in f. The mass encases the subclavian artery (S) and the T1 nerve root but merely abuts the C8 nerve root, and the higher nerve roots are preserved. Despite these findings of limited invasion of the vertebral body and brachial plexus, the tumor would have been eligible for surgical resection if distant metastases (not shown) had not been found.
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Figure 2f. Superior sulcus tumor in a 48-year-old man without neurologic signs in the left upper extremity but with left interscapular chest wall pain suggestive of T1 nerve root invasion. (a) Frontal chest radiograph shows a soft-tissue mass in the left lung apex. (b, c) Axial CT images obtained with soft-tissue (b) and bone (c) windows at the level of the thoracic inlet depict a superior sulcus tumor (SST) with focal destruction of the T2 vertebral body (arrowhead) and probable extension into the T2–3 neurovertebral foramen (arrow in b). (d) Axial T1-weighted MR image at the same level as b helps confirm that the mass (SST) has invaded the T2 vertebral body (arrowhead) and extends into the T2–3 neurovertebral foramen (arrow) as far as the extradural space. (e, f) Comparison of sagittal T1-weighted MR images at the level of the interscalene space before (e) and after (f) the intravenous administration of gadolinium shows enhancement of the mass (SST) in f. The mass encases the subclavian artery (S) and the T1 nerve root but merely abuts the C8 nerve root, and the higher nerve roots are preserved. Despite these findings of limited invasion of the vertebral body and brachial plexus, the tumor would have been eligible for surgical resection if distant metastases (not shown) had not been found.
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Absolute contraindications to surgery (Table 1) include invasion of the brachial plexus roots or trunks at levels above T1 (2,3), invasion of more than 50% of a vertebral body (3,4), and invasion of the esophagus or trachea (3). In addition, N2 (mediastinal) or N3 (contralateral supraclavicular) nodal metastases (5–7) and distant metastatic disease are absolute contraindications to surgery (Fig 3).
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Figure 3a. Superior sulcus tumor in a 59-year-old man with right shoulder pain and no neurologic signs. (a) Axial MR image at the level of the thoracic inlet shows a soft-tissue mass (SST) in the right lung apex, immediately abutting the right subclavian artery (*). T = trachea. (b) Coronal MR image shows that the mass (SST) has displaced the subclavian artery (arrowheads) superiorly. T = trachea. (c–e) Sagittal contrast-enhanced T1-weighted MR images through the right superior sulcus show that the mass (SST) is necrotic and encases the origins of the right subclavian and vertebral arteries (* in c and d). The clear fat plane between the mass and the roots (c, d) and trunks (e) of the brachial plexus would be indicative of possible resectability of the tumor, but extension into the anterior scalene muscle (white arrowheads in d) in the vicinity of the phrenic nerve (black arrowhead in d) precludes surgery. L, M, U = lower, middle, and upper trunks of brachial plexus; R = first rib; T1 = T1 nerve root. (f) Coronal image from positron emission tomography (PET)/CT shows increased uptake of fluorine-18 fluorodeoxyglucose (FDG) in the peripheral aspect of the mass (arrowhead) as well as FDG-avid subcarinal lymphadenopathy (arrow), a finding indicative of N2 metastatic disease and, thus, of tumor nonresectability.
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Figure 3b. Superior sulcus tumor in a 59-year-old man with right shoulder pain and no neurologic signs. (a) Axial MR image at the level of the thoracic inlet shows a soft-tissue mass (SST) in the right lung apex, immediately abutting the right subclavian artery (*). T = trachea. (b) Coronal MR image shows that the mass (SST) has displaced the subclavian artery (arrowheads) superiorly. T = trachea. (c–e) Sagittal contrast-enhanced T1-weighted MR images through the right superior sulcus show that the mass (SST) is necrotic and encases the origins of the right subclavian and vertebral arteries (* in c and d). The clear fat plane between the mass and the roots (c, d) and trunks (e) of the brachial plexus would be indicative of possible resectability of the tumor, but extension into the anterior scalene muscle (white arrowheads in d) in the vicinity of the phrenic nerve (black arrowhead in d) precludes surgery. L, M, U = lower, middle, and upper trunks of brachial plexus; R = first rib; T1 = T1 nerve root. (f) Coronal image from positron emission tomography (PET)/CT shows increased uptake of fluorine-18 fluorodeoxyglucose (FDG) in the peripheral aspect of the mass (arrowhead) as well as FDG-avid subcarinal lymphadenopathy (arrow), a finding indicative of N2 metastatic disease and, thus, of tumor nonresectability.
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Figure 3c. Superior sulcus tumor in a 59-year-old man with right shoulder pain and no neurologic signs. (a) Axial MR image at the level of the thoracic inlet shows a soft-tissue mass (SST) in the right lung apex, immediately abutting the right subclavian artery (*). T = trachea. (b) Coronal MR image shows that the mass (SST) has displaced the subclavian artery (arrowheads) superiorly. T = trachea. (c–e) Sagittal contrast-enhanced T1-weighted MR images through the right superior sulcus show that the mass (SST) is necrotic and encases the origins of the right subclavian and vertebral arteries (* in c and d). The clear fat plane between the mass and the roots (c, d) and trunks (e) of the brachial plexus would be indicative of possible resectability of the tumor, but extension into the anterior scalene muscle (white arrowheads in d) in the vicinity of the phrenic nerve (black arrowhead in d) precludes surgery. L, M, U = lower, middle, and upper trunks of brachial plexus; R = first rib; T1 = T1 nerve root. (f) Coronal image from positron emission tomography (PET)/CT shows increased uptake of fluorine-18 fluorodeoxyglucose (FDG) in the peripheral aspect of the mass (arrowhead) as well as FDG-avid subcarinal lymphadenopathy (arrow), a finding indicative of N2 metastatic disease and, thus, of tumor nonresectability.
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Figure 3d. Superior sulcus tumor in a 59-year-old man with right shoulder pain and no neurologic signs. (a) Axial MR image at the level of the thoracic inlet shows a soft-tissue mass (SST) in the right lung apex, immediately abutting the right subclavian artery (*). T = trachea. (b) Coronal MR image shows that the mass (SST) has displaced the subclavian artery (arrowheads) superiorly. T = trachea. (c–e) Sagittal contrast-enhanced T1-weighted MR images through the right superior sulcus show that the mass (SST) is necrotic and encases the origins of the right subclavian and vertebral arteries (* in c and d). The clear fat plane between the mass and the roots (c, d) and trunks (e) of the brachial plexus would be indicative of possible resectability of the tumor, but extension into the anterior scalene muscle (white arrowheads in d) in the vicinity of the phrenic nerve (black arrowhead in d) precludes surgery. L, M, U = lower, middle, and upper trunks of brachial plexus; R = first rib; T1 = T1 nerve root. (f) Coronal image from positron emission tomography (PET)/CT shows increased uptake of fluorine-18 fluorodeoxyglucose (FDG) in the peripheral aspect of the mass (arrowhead) as well as FDG-avid subcarinal lymphadenopathy (arrow), a finding indicative of N2 metastatic disease and, thus, of tumor nonresectability.
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Figure 3e. Superior sulcus tumor in a 59-year-old man with right shoulder pain and no neurologic signs. (a) Axial MR image at the level of the thoracic inlet shows a soft-tissue mass (SST) in the right lung apex, immediately abutting the right subclavian artery (*). T = trachea. (b) Coronal MR image shows that the mass (SST) has displaced the subclavian artery (arrowheads) superiorly. T = trachea. (c–e) Sagittal contrast-enhanced T1-weighted MR images through the right superior sulcus show that the mass (SST) is necrotic and encases the origins of the right subclavian and vertebral arteries (* in c and d). The clear fat plane between the mass and the roots (c, d) and trunks (e) of the brachial plexus would be indicative of possible resectability of the tumor, but extension into the anterior scalene muscle (white arrowheads in d) in the vicinity of the phrenic nerve (black arrowhead in d) precludes surgery. L, M, U = lower, middle, and upper trunks of brachial plexus; R = first rib; T1 = T1 nerve root. (f) Coronal image from positron emission tomography (PET)/CT shows increased uptake of fluorine-18 fluorodeoxyglucose (FDG) in the peripheral aspect of the mass (arrowhead) as well as FDG-avid subcarinal lymphadenopathy (arrow), a finding indicative of N2 metastatic disease and, thus, of tumor nonresectability.
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Figure 3f. Superior sulcus tumor in a 59-year-old man with right shoulder pain and no neurologic signs. (a) Axial MR image at the level of the thoracic inlet shows a soft-tissue mass (SST) in the right lung apex, immediately abutting the right subclavian artery (*). T = trachea. (b) Coronal MR image shows that the mass (SST) has displaced the subclavian artery (arrowheads) superiorly. T = trachea. (c–e) Sagittal contrast-enhanced T1-weighted MR images through the right superior sulcus show that the mass (SST) is necrotic and encases the origins of the right subclavian and vertebral arteries (* in c and d). The clear fat plane between the mass and the roots (c, d) and trunks (e) of the brachial plexus would be indicative of possible resectability of the tumor, but extension into the anterior scalene muscle (white arrowheads in d) in the vicinity of the phrenic nerve (black arrowhead in d) precludes surgery. L, M, U = lower, middle, and upper trunks of brachial plexus; R = first rib; T1 = T1 nerve root. (f) Coronal image from positron emission tomography (PET)/CT shows increased uptake of fluorine-18 fluorodeoxyglucose (FDG) in the peripheral aspect of the mass (arrowhead) as well as FDG-avid subcarinal lymphadenopathy (arrow), a finding indicative of N2 metastatic disease and, thus, of tumor nonresectability.
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The presence of nodal metastases (N1–N3) is associated with a much poorer survival than is nonmetastatic (N0) disease (6–9).Mediastinal lymph node metastases are reported to occur in up to 20% of patients with superior sulcus tumors (10), and, accordingly, mediastinoscopy is advisable in all potential surgical candidates before treatment, both for staging purposes and for determining the extent of lymph node dissection at the time of surgery. However, whereas mediastinal (N2) and contralateral supraclavicular (N3) nodal metastases represent absolute contraindications to surgery, hilar (N1) and ipsilateral supraclavicular (N3) nodal metastases constitute relative contraindications, because both can be successfully resected with the primary tumor and do not necessarily preclude long-term survival (9,11). PET/CT may usefully complement mediastinoscopy by depicting unsuspected nodal metastases (Fig 3) in sites that are not accessible with a transcervical approach (12,13); in such patients, anterior mediastinoscopy, video-assisted thoracoscopic surgery, or endobronchial ultra-sonographically guided biopsy may be necessary to determine nodal status.
Other relative contraindications include invasion of the subclavian vessels, which is often difficult to establish at imaging prior to surgery. If the subclavian vein is involved, it can be ligated and resected easily along with the tumor, since collateral venous pathways usually have developed by the time of diagnosis. Tumors that have invaded the subclavian artery are also technically resectable, but resection must be accompanied by vascular reconstruction with a polytetrafluoroethylene graft. A tumor with intraforaminal extension is potentially resectable unless there is an anterior spinal artery that enters the spinal canal at that level (3,14). Similarly, tumors that have invaded less than 50% of a vertebral body may be resectable, but their resection often requires a combined thoracic and neurosurgical approach (2,4, 15). Last, invasion of the common carotid artery or vertebral artery represents another relative contraindication to surgery. These vessels often have to be ligated to achieve complete resection of a locally invasive carcinoma. However, if there is significant atherosclerotic disease of the contralateral vessels, resection may not be feasible (3). In such instances, CT or MR imaging may be the first examination that alerts the surgeon to the presence of contralateral atherosclerosis.
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Imaging Features
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Radiography
Radiography is usually the first imaging evaluation performed in patients with nonspecific shoulder pain or a cough. Unfortunately, because of their location in the lung apices, superior sulcus tumors are difficult to detect. The tumor often appears as a subtle soft-tissue mass that may be confused with benign apical pleural thickening (Fig 2) (16). The presence of associated rib or vertebral body destruction may be difficult to ascertain on the basis of radiographs. In most patients, thoracic CT is necessary to determine whether a mass is present.
Thoracic CT
The main objectives of CT in patients with a superior sulcus tumor are to confirm the presence of a pulmonary mass, to allow accurate staging of disease (through the detection of nodal and pulmonary metastases), and to guide biopsy. In the superior sulcus, CT is the best modality for depicting bone abnormalities adjacent to the primary mass, such as rib and vertebral body erosion (Fig 2)—information that may influence the surgical approach taken and the extent of the resection. CT also is useful for assessing the patency of subclavian vessels. In patients with a history of coronary artery bypass surgery, CT may alert the surgeon to the presence and site of internal mammary artery bypass grafts, information that may be of critical importance if a resection of the subclavian artery is being considered.
Although CT is the ideal modality for detecting osseous erosion, it has only a limited ability to depict tumor extension into the neurovertebral foramina and the spinal canal (2) (Figs 1, 2). The assessment of brachial plexus involvement also is difficult at CT because of the limited contrast resolution (compared with that at MR imaging) and frequently because of streak artifact caused by the presence of contrast material in the subclavian vessels. For these reasons, we reserve CT for evaluating the bones and intrathoracic structures (particularly the mediastinum) and use MR imaging to evaluate the primary tumor and its anatomic extension in the superior sulcus.
MR Imaging
MR imaging is the optimal modality for evaluating tumors of the superior sulcus and determining their resectability. Its advantages include multiplanar capabilities, superior contrast resolution (in comparison with that of other modalities), and a lack of ionizing radiation. MR imaging is superior to CT in depicting tumor invasion of the chest wall, extension into the neurovertebral foramina and spinal canal, and involvement of the brachial plexus (Figs 1–3) (16–20). Although tumor involvement of these structures may be inferred from the CT findings in many cases, MR imaging allows the direct depiction of such involvement and therefore improves reader confidence (18). Disadvantages of MR imaging include its limited availability compared with that of CT, as well as longer image acquisition times and increased susceptibility to motion artifact and patient claustrophobia.
At our institution, MR imaging of superior sulcus tumors is performed by using a modification of a protocol described by Demondion et al (21) (Table 2). Both cardiac gating and respiratory gating are used to minimize motion and pulsation artifacts (Fig 4). To optimize sensitivity for the small structures in the thoracic inlet, such as the brachial plexus nerve roots and trunks, imaging is performed by using a neurovascular neck coil. A comprehensive study includes T1- and T2-weighted imaging of the ipsilateral thoracic inlet in the sagittal, axial, and coronal planes. Sagittal T1-weighted images are acquired by using thin sections (3.0 mm) with a minimal gap (0.3 mm); sagittal T2-weighted images are acquired by using fat suppression sequences and larger section thicknesses (6.0 mm) because of the poorer signal-to-noise ratio. Sagittal T1-weighted sequences provide the most-detailed anatomic information and should be performed first. T2-weighted sequences are sometimes useful for obtaining improved depiction of the primary tumor and for detecting surrounding inflammation, but in most cases they do not contribute any additional important information about resectability (18). Imaging in the axial plane is best for localization of the primary tumor in the thoracic inlet and for visualization of the spinal canal, the neurovertebral foramina, and the nerve rami (Figs 1, 2) (19). Imaging in the sagittal plane is optimal for depicting the components of the brachial plexus, the subclavian vessels, and the posterior arcs of the ribs in cross sections (Figs 1–3). Unfortunately, because of partial volume averaging effects, it is difficult to make a confident diagnosis of brachial plexus invasion on the basis of coronal images alone, and, in agreement with other investigators (19), we have found coronal images to be the least useful. However, they do allow an assessment of the cephalic limits of tumor extension (Fig 3b) and may depict the brachial plexus roots.
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Figure 4a. Respiratory motion artifact. (a) Axial T1-weighted MR image acquired without respiratory gating shows blurring of the margins of a right superior sulcus tumor (SST) and a linear artifact in the center of the mass. (b) Axial T1-weighted MR image acquired with respiratory gating in the same patient, at the same level, shows clearer delineation of the tumor margins with evidence of tumor extension into the chest wall (arrow). T = trachea, V = vertebral body.
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Figure 4b. Respiratory motion artifact. (a) Axial T1-weighted MR image acquired without respiratory gating shows blurring of the margins of a right superior sulcus tumor (SST) and a linear artifact in the center of the mass. (b) Axial T1-weighted MR image acquired with respiratory gating in the same patient, at the same level, shows clearer delineation of the tumor margins with evidence of tumor extension into the chest wall (arrow). T = trachea, V = vertebral body.
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A rectangular field of view is used according to the patient size, with the phase-encoding direction along the short axis to help shorten the image acquisition time. In the sagittal plane, the volume of interest extends from the midline of the vertebral bodies to the retropectoral region (lateral to the costovertebral space); in the axial plane, from the upper cervical spine to the upper thoracic spine; and in the coronal plane, from anterior to posterior, to include the entire thoracic inlet. The volume of interest may have to be foreshortened to achieve shorter image acquisition time, particularly in patients who are short of breath or who have uncontrolled shoulder pain. In such cases, knowledge of the most likely location of the tumor, based on the patient’s symptomatology or on CT findings, may allow more localized tailoring of the examination. In all patients, T1-weighted sagittal sequences should be performed first in case imaging has to be interrupted or aborted, because the sagittal images alone may provide sufficient diagnostic information.
The subclavian vessels appear as flow voids on spin-echo images, and their relationship with the components of the brachial plexus is well depicted in most patients without the use of intravenous gadolinium. A contrast medium is usually used in patients in whom vascular invasion or intraforaminal extension is suspected to be present; in patients who have undergone neoadjuvant therapy before a planned resection, in whom posttreatment fibrosis may result in blurring of the intermuscular fat planes and difficulty in visualizing the primary tumor; and in patients in whom a recurrence is suspected after definitive treatment. In the latter two situations, abnormal enhancement may signify a viable persistent or recurrent tumor, although enhancement also may be seen in benign fibrotic tissue (Fig 5).
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Figure 5a. Imaging findings in a 61-year-old woman after surgical resection of a superior sulcus tumor and adjuvant radiation therapy. (a) Axial CT image at the level of the thoracic inlet shows soft tissue in the right lung apex (arrowheads). (b–d) Axial (b) and sagittal (c, d) MR images of the right superior sulcus before (c) and after (d) the administration of gadolinium show an enhancing soft-tissue mass (M) in the right superior sulcus (arrow in b), abutting the right subclavian artery (*). (e) Axial PET/CT image at the same level as a shows diffuse low-grade FDG uptake within the mass (arrow). Because imaging surveillance over the next 4 years helped confirm the stability of the mass and the patient remained asymptomatic, these findings were deemed consistent with radiation therapy–induced fibrosis.
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Figure 5b. Imaging findings in a 61-year-old woman after surgical resection of a superior sulcus tumor and adjuvant radiation therapy. (a) Axial CT image at the level of the thoracic inlet shows soft tissue in the right lung apex (arrowheads). (b–d) Axial (b) and sagittal (c, d) MR images of the right superior sulcus before (c) and after (d) the administration of gadolinium show an enhancing soft-tissue mass (M) in the right superior sulcus (arrow in b), abutting the right subclavian artery (*). (e) Axial PET/CT image at the same level as a shows diffuse low-grade FDG uptake within the mass (arrow). Because imaging surveillance over the next 4 years helped confirm the stability of the mass and the patient remained asymptomatic, these findings were deemed consistent with radiation therapy–induced fibrosis.
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Figure 5c. Imaging findings in a 61-year-old woman after surgical resection of a superior sulcus tumor and adjuvant radiation therapy. (a) Axial CT image at the level of the thoracic inlet shows soft tissue in the right lung apex (arrowheads). (b–d) Axial (b) and sagittal (c, d) MR images of the right superior sulcus before (c) and after (d) the administration of gadolinium show an enhancing soft-tissue mass (M) in the right superior sulcus (arrow in b), abutting the right subclavian artery (*). (e) Axial PET/CT image at the same level as a shows diffuse low-grade FDG uptake within the mass (arrow). Because imaging surveillance over the next 4 years helped confirm the stability of the mass and the patient remained asymptomatic, these findings were deemed consistent with radiation therapy–induced fibrosis.
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Figure 5d. Imaging findings in a 61-year-old woman after surgical resection of a superior sulcus tumor and adjuvant radiation therapy. (a) Axial CT image at the level of the thoracic inlet shows soft tissue in the right lung apex (arrowheads). (b–d) Axial (b) and sagittal (c, d) MR images of the right superior sulcus before (c) and after (d) the administration of gadolinium show an enhancing soft-tissue mass (M) in the right superior sulcus (arrow in b), abutting the right subclavian artery (*). (e) Axial PET/CT image at the same level as a shows diffuse low-grade FDG uptake within the mass (arrow). Because imaging surveillance over the next 4 years helped confirm the stability of the mass and the patient remained asymptomatic, these findings were deemed consistent with radiation therapy–induced fibrosis.
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Figure 5e. Imaging findings in a 61-year-old woman after surgical resection of a superior sulcus tumor and adjuvant radiation therapy. (a) Axial CT image at the level of the thoracic inlet shows soft tissue in the right lung apex (arrowheads). (b–d) Axial (b) and sagittal (c, d) MR images of the right superior sulcus before (c) and after (d) the administration of gadolinium show an enhancing soft-tissue mass (M) in the right superior sulcus (arrow in b), abutting the right subclavian artery (*). (e) Axial PET/CT image at the same level as a shows diffuse low-grade FDG uptake within the mass (arrow). Because imaging surveillance over the next 4 years helped confirm the stability of the mass and the patient remained asymptomatic, these findings were deemed consistent with radiation therapy–induced fibrosis.
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CT versus MR Imaging
There have been a limited number of prospective studies with small numbers of patients in which the relative merits of CT and MR imaging of the superior sulcus were compared (18–20). In all of these studies, the investigators found MR imaging to be superior to CT for the assessment of brachial plexus invasion, primarily because of the multiplanar capabilities of MR imaging. However, these studies were conducted in the late 1980s and early 1990s, when CT technology was limited to single-section scanning with image reconstruction in the axial plane only; furthermore, information regarding the correlation of imaging findings with surgical findings is limited. It is probable that the more recently developed multi-detector CT technology—which enables the reconstruction of high-quality multiplanar images with isotropic voxels—may be used to evaluate the structures of the superior sulcus with a greater degree of accuracy than was reported for CT previously. However, MR imaging remains the reference standard.
PET/CT
PET/CT is useful for detecting nodal and distant metastases at baseline staging in patients with bronchogenic carcinomas (Fig 3) (12,13,22–26), and it is recommended in all patients with a superior sulcus tumor who are potential surgical candidates. PET/CT is also useful in patients in whom the tumor is suspected to have recurred after definitive therapy; in such patients, a finding of increased uptake of FDG in the superior sulcus may guide biopsy and help confirm the diagnosis of persistent or recurrent disease.
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Assessment of Tumor Response
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An imaging evaluation of patients who are undergoing multimodality therapy often is requested to assess the response of a tumor after the completion of radiation or chemotherapy and to reevaluate the tumor for resectability. In such patients, induction radiation therapy usually results in extensive tissue fibrosis and blurring of the intermuscular fat planes, processes that make it difficult to visualize superior sulcus tumors without the use of an intravenous contrast medium. However, at MR imaging, the administration of gadolinium causes enhancement of both the primary tumor and any surrounding fibrotic tissue, making it difficult to determine the presence and extension of residual tumor tissue. In several surgical series, a poor correlation was observed between imaging findings and the pathologic response to induction therapy, with residual "masses" seen at MR imaging or CT often corresponding to scar tissue instead of viable tumor tissue (2,27,28) (Fig 5). In a recent Southwest Oncology Group trial, 65% of the patients who were considered to have stable disease according to CT criteria actually had either a complete response or minimal residual disease after therapy, when resection specimens were analyzed (28). For this reason, imaging findings in the thoracic inlet following neoadjuvant treatment should not be used as criteria for determining the resectability of the residual tumor.
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Detection of Tumor Recurrence
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Tumor recurrence may be suspected because of recurrent shoulder pain or new or progressive nerve palsy, signs associated with mediastinal invasion (diaphragmatic palsy, hoarseness, superior vena cava compression), or because of progressive weight loss and general debility after definitive treatment. For the reasons described earlier, MR images often provide poor information about early-stage tumor recurrence because they allow only limited discrimination between post-therapy fibrosis and residual or recurrent tumor. On CT images, new bone erosion is a suspicious finding that is indicative of probable local tumor recurrence. On PET/CT images, a new focal site of increased FDG uptake may be indicative of tumor recurrence and may be used to guide biopsy (Fig 6). However, a minimal or intermediate degree of FDG uptake is a nonspecific finding that commonly is observed in regions of posttreatment inflammation, which may persist for years after radiation therapy (Fig 5). Imaging findings therefore should be correlated with the patient’s symptoms and signs and with previous studies. A fine-needle aspiration biopsy often is necessary to obtain a definitive diagnosis.
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Figure 6a. Local recurrence after definitive radiation therapy of a superior sulcus tumor in a 62-year-old man. (a) Axial CT image obtained at the level of the thoracic inlet shows an ill-defined soft-tissue mass in the left lung apex. The mass encases the left vertebral artery (arrow) and is associated with a subtle focal irregularity of the second rib (arrowheads). (b, c) Axial (b) and sagittal (c) MR images of the left superior sulcus show the mass (M) encasing the origin of the left vertebral artery (*) and the left subclavian artery and extending posteriorly toward the T2–3 neurovertebral foramen (arrow). V = vertebra. (d) Axial PET/CT image at the same level as a shows a focal area of increased FDG uptake in the posterior portion of the mass (arrow).
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Figure 6b. Local recurrence after definitive radiation therapy of a superior sulcus tumor in a 62-year-old man. (a) Axial CT image obtained at the level of the thoracic inlet shows an ill-defined soft-tissue mass in the left lung apex. The mass encases the left vertebral artery (arrow) and is associated with a subtle focal irregularity of the second rib (arrowheads). (b, c) Axial (b) and sagittal (c) MR images of the left superior sulcus show the mass (M) encasing the origin of the left vertebral artery (*) and the left subclavian artery and extending posteriorly toward the T2–3 neurovertebral foramen (arrow). V = vertebra. (d) Axial PET/CT image at the same level as a shows a focal area of increased FDG uptake in the posterior portion of the mass (arrow).
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Figure 6c. Local recurrence after definitive radiation therapy of a superior sulcus tumor in a 62-year-old man. (a) Axial CT image obtained at the level of the thoracic inlet shows an ill-defined soft-tissue mass in the left lung apex. The mass encases the left vertebral artery (arrow) and is associated with a subtle focal irregularity of the second rib (arrowheads). (b, c) Axial (b) and sagittal (c) MR images of the left superior sulcus show the mass (M) encasing the origin of the left vertebral artery (*) and the left subclavian artery and extending posteriorly toward the T2–3 neurovertebral foramen (arrow). V = vertebra. (d) Axial PET/CT image at the same level as a shows a focal area of increased FDG uptake in the posterior portion of the mass (arrow).
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Figure 6d. Local recurrence after definitive radiation therapy of a superior sulcus tumor in a 62-year-old man. (a) Axial CT image obtained at the level of the thoracic inlet shows an ill-defined soft-tissue mass in the left lung apex. The mass encases the left vertebral artery (arrow) and is associated with a subtle focal irregularity of the second rib (arrowheads). (b, c) Axial (b) and sagittal (c) MR images of the left superior sulcus show the mass (M) encasing the origin of the left vertebral artery (*) and the left subclavian artery and extending posteriorly toward the T2–3 neurovertebral foramen (arrow). V = vertebra. (d) Axial PET/CT image at the same level as a shows a focal area of increased FDG uptake in the posterior portion of the mass (arrow).
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Summary
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Tumors of the superior sulcus are best managed by using a multimodality approach in which surgery is combined with radiation therapy, with or without chemotherapy. Imaging is crucial for the initial staging of superior sulcus tumors, for determining the surgical approach, and for planning radiation treatment. Because of the close and complex relationships among the anatomic structures in the thoracic inlet, optimal imaging requires a multiplanar and multimodality approach in which information obtained from CT, alone or with PET, is combined with that obtained from MR imaging. The usefulness of the imaging findings is enhanced by the radiologist’s knowledge of the patient’s symptoms and thorough understanding of the therapeutic options available. To ensure appropriate clinical decision making and optimal outcomes, multidisciplinary meetings of neuro- and thoracic surgeons, radiation and medical oncologists, and radiologists should be held to discuss the patient’s signs and symptoms, imaging findings, and management options.
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Footnotes
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Abbreviations: FDG = fluorodeoxyglucose
See also the article by Bruzzi et al (pp 551–560) 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 1: Anatomy, Clinical Manifestations, and Management
- John F. Bruzzi, Ritsuko Komaki, Garrett L. Walsh, Mylene T. Truong, Gregory W. Gladish, Reginald F. Munden, and Jeremy J. Erasmus
RadioGraphics 2008 28: 551-560.
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Abstract
Introduction
