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The Oncologist, Vol. 9, No. 5, 550-555, September 2004; doi:10.1634/theoncologist.9-5-550
© 2004 AlphaMed Press

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Superior Sulcus Tumors: A Mini-Review

Victor C. Archiea, Charles R. Thomas, Jr.b

a Department of Radiation Oncology, UCLA Jonsson Cancer Center, Los Angeles, California, USA; b Department of Radiation Oncology and Division of Medical Oncology/Department of Medicine, University of Texas Health Science Center at San Antonio, San Antonio Cancer Institute, San Antonio, Texas, USA

Correspondence: Charles R. Thomas Jr., M.D., Department of Radiation Oncology, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, Texas 78229, USA. Telephone: 210-616-5684; Fax: 210-949-5085; e-mail: cthomas{at}ctrc.net; Website: http://www.uthscsa.edu/radiationoncology


   LEARNING OBJECTIVES
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 Summary
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After completing this course, the reader will be able to:

  1. Describe the diagnostic work-up for superior sulcus (Pancoast) tumors of the lung.
  2. List the major prognostic factors pertaining to outcome in patients with superior sulcus (Pancoast) tumors.
  3. Discuss the recent (SWOG 94-16) and current (SWOG-0220) intergroup trials for superior sulcus (Pancoast) tumors.

Access and take the CME test online and receive 1 hour of AMA PRA category 1 credit at CME.TheOncologist.com


   ABSTRACT
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 Abstract
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 Treatment
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The management and outcome for superior sulcus tumors have remained unchanged for 40 years. The rarity of these tumors has led to varying treatment techniques spanning decades, from which no solid conclusions can be drawn. Recent advances in combined-modality therapy have offered the first inkling that a paradigm shift is on the horizon. Here, we review the history and new advances in treating this challenging pulmonary neoplasm.

Key Words. Pancoast • Superior sulcus • Non-small cell lung cancer • Combined-modality


   HISTORY
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 Abstract
 History
Diagnosis and Work-up
 Treatment
 Current Recommendations and...
 Summary
 References
 
In 1924, Pancoast [1] reported the clinical and radiographic findings associated with superior sulcus tumors. He initially thought that these tumors arose from epithelial rest cells from the fifth brachial cleft. Eight years later, Tobias [2] and Pancoast [3] simultaneously, correctly recognized that bronchogenic carcinoma was the primary cause of this syndrome.

Superior sulcus tumors usually arise in the apex of the lung and may invade the second and third ribs, the brachial plexus, the subclavian vessels, the stellate ganglion, and adjacent vertebral bodies [4]. Pancoast syndrome is characterized by pain, which may arise in the shoulder or chest wall or radiate to the neck. Pain characteristically radiates to the ulnar surface of the hand. Horner’s syndrome, which is composed of ptosis, meiosis, and anhydrosis, results from invasion of the paravertebral sympathetic chain. Weakness and atrophy of the hand and parasthesias are a common clinical finding resulting from invasion into the C8 and T1 roots of the brachial plexus. More infrequent manifestations include supraclavicular adenopathy, superior vena cava syndrome, and involvement of the phrenic or laryngeal nerves [5].

Prior to the 1950s, superior sulcus tumors were uniformly fatal. Chardack and MacCallum [6] reported the first successful treatment with resection followed by postoperative radiation. Paulson, using preoperative radiation followed by surgical resection, published the first series, which included 18 patients, in 1966 [7].

Non-small cell lung cancer is the primary etiology associated with radiographic abnormalities in the superior sulcus. However, only 5% of non-small cell lung cancers present as superior sulcus tumors. Other causes of superior sulcus tumors include metastatic solid tumors [8–10] and unusual presentations of hematological malignancies, as well as infectious diseases, a cervical rib, and pulmonary amyloid nodules [5].


   DIAGNOSIS AND WORK-UP
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 Diagnosis and Work-up
Treatment
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The pain associated with superior sulcus tumors often leads to a prolonged interval from initial clinical presentation to diagnosis. Routine chest radiography leads to further studies. Superior sulcus tumors are peripherally located and characterized by a spiculated density in the apices of the lung with or without evidence of mediastinal abnormality. Due to their unique location, bronchoscopy and cytology are only effective in establishing diagnosis in 10%–20% of cases [11]. Percutaneous needle biopsy via ultrasound or under computerized tomography (CT) guidance is generally sufficient to make the diagnosis.

Work-up includes CT scans of the chest and abdomen, pulmonary function testing, a CBC, liver function tests, evaluation of electrolytes, and a bone scan. A mediastinoscopy should be performed, as N2 disease has been shown to be a poor prognostic factor [12–15]. Therefore, mediastinoscopy is mandatory and crucial in triaging those patients to the operative versus nonoperative approach. A magnetic resonance imaging (MRI) scan of the brain is not routine but is certainly warranted if symptoms are present. In addition to these routine studies for staging non-small cell lung cancer, MRI of the chest [16] and magnetic resonance angiography [17] add important information regarding tumor extent and surgical resectability. Information can be gained regarding involvement of the brachial plexus, neural foramina, and vertebral bodies, and arterial or venous involvement. The use of positron emission tomography (PET) is not clearly defined in this subset of tumors but is used widely in the staging of non-small cell lung cancer in general. Since the risk of lymphadenopthy is small, distant metastasis may better be discerned with a less expensive bone scan.


   TREATMENT
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Surgery consists of a posteriolateral [18–20] approach, an anterior transclavicular [21, 22] approach, partial sternotomy [23], and finally a combined vertebrectomy and reconstruction combined with chest wall reconstruction when the vertebral body is involved [24–26]. Vascular involvement and vertebral body involvement have historically been contraindications to surgical intervention; however, with advances in surgical techniques and better preoperative staging, tumors that were deemed unresectable may now undergo resection. Although technically feasible, the utility of surgery in the subset of patients with vertebral body and vascular invasion remains to be proven [14].

Radiation therapy (RT) has been used as a single modality as well as in multimodality therapy. Monotherapy results are generally poor, however, and a 5-year survival rate of 23% has been reported [27, 28]. Variations in dose, treatment technique, and staging and the lack of reporting of treatment-related morbidity have made the effectiveness of radiation therapy difficult to assess. Modern radiotherapy planning techniques allow a more accurate delivery of the radiation dose and the potential to escalate the dose without increasing morbidity. Researchers at M.D. Anderson Cancer Center have demonstrated that a dose of 66 Gy led to superior survival in patients who received definitive RT with sequential or concurrent chemotherapy [29]. The dose-limiting structures include the spinal cord and the brachial plexus. Doses of 45 Gy, for the former, and 60 Gy, for the latter, can be delivered with complications in <5% of patients [30].

Alternate forms of radiation therapy have been used with and without external beam radiotherapy. Techniques using brachytherapy [31] and intraoperative radiotherapy [32] have shown promising results in highly selected patients. These techniques are not widely available, nor is there information regarding long-term morbidity.

Chemotherapy as a single modality has historically been reserved for palliation in patients with metastatic disease. Complete response rates with single- or multiagent chemotherapy are in the single digits in the treatment of non-small cell lung cancer. However, as induction therapy prior to surgery or definitive radiation therapy [33] or in the setting with concurrent radiation therapy [34], its role is more clearly defined.

Combined Modality Therapy
In the first reported series of patients, Paulson [7] used radiotherapy prior to surgery. The rationale for this approach included improving resectability, decreasing tumor seeding at surgery, blocking lymphatic channels (and therefore potentially limiting metastasis), and maximizing local control. The doses of radiation used in that trial ranged from 30–45 Gy. Historically, doses greater than 55 Gy have been associated with higher levels of operative morbidity and mortality. With modern day radiation techniques, most specifically three-dimensional conformal treatments, it is clear that doses of 50–60 Gy can be delivered; however, the utility of dose escalation in the preoperative setting is unclear.

Several authors have evaluated the sequencing of surgery and radiotherapy [13, 28, 35]. These retrospective reviews did not find a difference in outcomes if clear margins could be obtained on surgical resection. Care must be taken to evaluate these data because of the potential for bias in retrospective data. Despite improvements in imaging modalities, determining resectability can be extremely difficult. Therefore, most authors recommend preoperative therapy prior to any attempt at resection. Approximately 10%–20% of patients exhibit pN2 disease. The 5-year survival rate in this group is <10%. These facts underscore the need for meticulous preoperative staging [36].

Concurrent Chemotherapy and Radiation Followed by Surgery
As stated previously, the role of chemotherapy has been clearly defined in the treatment of locally advanced non-small cell lung cancer and has been shown to be superior to radiation therapy alone. The phase II Southwestern Oncology Group (SWOG) 94-16 trial [37, 38] evaluated the role of concurrent cisplatin (Platinol®; Bristol-Myers Squibb) at a dose of 50 mg/m2 on days 1, 8, 29, and 36 and etoposide (Etopophos®; Bristol-Myers Squibb; Princeton, NJ) at a dose of 50 mg/m2 on days 1–5 and days 29–33 with 45 Gy of TRT over 5 weeks followed by two additional cycles of chemotherapy in mediastinoscopy-negative patients with superior sulcus tumors in a multi-institutional setting. Those authors demonstrated that this therapy was associated with acceptable morbidity and mortality, and that complete resection rates of 92% where obtainable with this regimen. Sixty-six percent of those who went on to surgery had pathologic complete responses (36%) or minimal microscopic disease (30%) on resection. Of the patients who completed induction therapy and went on to surgery, the 2-year survival rates were 55% for all patients and 70% for those who underwent complete resection [38, 39]. Updated results noted a 33-month median survival and a 5-year overall survival rate of 41% for the total cohort [39]. The Japan Clinical Oncology Group (JCOG) protocol 9806 is similar to the North American intergroup effort (Table 1Go) [38–40].


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  		Table 1. Comparison of results of the JCOG-9806 and SWOG 94-16 trials in superior sulcus tumors
 
Wright et al. [41] from the Massachusetts General Hospital published a retrospective review of patients treated with different institutional protocols consisting of preoperative chemoradiation and radiation alone. The patients who received chemotherapy had a higher complete resection rate, higher pathologic complete response rate, lower local recurrence rate, and longer survival than patients treated with radiation alone. These results are consistent with current knowledge, but selection bias may have contributed to this result.

Complications

Surgery
Because of the retrospective nature of the literature and treatment intervals spanning decades, it is difficult to assess the true morbidity and mortality associated with treating patients with superior sulcus tumors. Operative mortality has ranged from 0%–14% in single institution studies [42, 43]; however, in the only multi-institutional study, SWOG 94-16, the mortality rate was 1.2%. Morbidity is more sparsely detailed but ranges from 7%–38%.

The primary perioperative complication is pneumonia. It has been hypothesized that poor pain control and chest wall instability lead to a decreased cough reflex and retention of secretions. Aggressive chest physiotherapy and adequate analgesia have significantly reduced the incidence of this complication. Other potential surgical complications include bronchopleural fistula, wound infection, hemothorax, chylothorax, pulmonary embolism, and wound dehiscence. In addition, complications related to vascular and neural structures have been noted. Vascular complications include puncture or tear and subclavian vein thrombosis. Horner’s syndrome may be caused by high dorsal root sympathatectomy and, not surprisingly, ulnar nerve dysfunction may result from damage to C8 and or T1.

Toxicity of Combined Modality Therapy
Shahian et al. [44] described neurologic dysfunction in 70% of long-term survivors treated with combined surgery and radiation. Pneumonitis is also a possibility when radiation is a part of therapy, and its incidence ranges from 0%–20% [45]. Although the exact mechanism is unknown, pneumonitis is much more likely to occur when attempts are made to treat the mediastinum, and the volume receiving 20 Gy (V20) becomes larger [46]. The total mean lung dose is another useful clinical measure used to estimate the risk of pneumonitis. If the dose is greater than or less than 20 Gy, the rates of pneumonitis are 8% and 24%, respectively [47].

Chemoradiotherapy is also associated with an increased risk of esophagitis. Byhardt and others reviewed five Radiation Therapy Oncology Group (RTOG) trials and found that grade 3 esophagitis (which includes severe dysphagia or odynophagia, dehydration or weight loss <15%, placement of a nasogastric tube, i.v. fluids, or hyperalimentation) occurs in 27%–55% of patients, depending on whether chemotherapy is given concurrently and based on the RT fractionation schedule [48]. Efforts to modulate this toxicity have proved ineffective to date in a randomized setting [49].

Few studies report morbidity and mortality in patients with superior sulcus tumors treated with chemotherapy. The SWOG trial reported a mortality of <1% in patients treated with neoadjuvant therapy.

Aside from mortality, it is certain that hematologic toxicities are greater in patients that receive chemotherapy. It must be kept in mind that a number of patients may discontinue therapy secondary to side effects or have an extended treatment time between neoadjuvant therapy and surgery, thus potentially harming outcome.


   CURRENT RECOMMENDATIONS AND FUTURE DIRECTIONS
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 Learning Objectives
 Abstract
 History
 Diagnosis and Work-up
 Treatment
 Current Recommendations and...
Summary
 References
 
Presently, patients who present with Pancoast lung lesions should undergo confirmation for malignancy, chest and brain CT (and/or MRI if there is clear brachial plexopathy) scans, and assessment of the mediastinum surgically (or, alternatively, via fluorodeoxyglucose [FDG]-PET), followed by a combined-modality therapeutic approach with a platinum-based doublet combination chemotherapy regimen (two cycles) with thoracic once-daily (standard fractionation) radiotherapy to a dose of 45 Gy in 1.8-Gy fractions (Monday–Friday). At the present time, TRT should be done with modern conformal techniques, while the use of intensity-modulated radiation therapy is unproven and not recommended for routine use. After restaging, if there is no evidence of progressive disease, then an attempt at surgical resection is mandated by an experienced thoracic surgeon (with the assistance of an orthopedic spine surgeon or neurosurgeon, as deemed necessary). For patients who are either unwilling and/or unable to undergo a trimodality approach, then definitive chemoradiotherapy to a total radiotherapy dose of around 60 Gy would be reasonable (especially since the brachial plexus is able to tolerate doses >60 Gy). More importantly, we believe that all patients should first be considered for treatment in a prospective clinical trial.

Based on the promising results of the SWOG 94-16 trial (40% 3-year survival rate), the SWOG has begun the SWOG-0220 trial. In that trial, patients with T3-4, N0, or N1 disease with no evidence of distant metastasis will receive cisplatin and etoposide concurrently with radiotherapy. After completion of induction treatment, patients that have had responses or stable disease will go on to surgical resection followed by three cycles of docetaxel (Taxotere®; Aventis Pharmaceuticals Inc.; Bridgewater, NJ), based on the results of the SWOG-9504 trial, which showed a median survival of 26 months and a 3-year survival rate of 37% [50]. If patients are unfit or refuse surgery, radiation will continue followed by the same chemotherapy regimen described above. It appears that consolidation therapy with taxanes is more tolerable than attempting to give more cisplatin following an induction concomitant modality approach.


   SUMMARY
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 Learning Objectives
 Abstract
 History
 Diagnosis and Work-up
 Treatment
 Current Recommendations and...
 Summary
References
 
Superior sulcus tumors present a unique challenge to thoracic oncologists [51]. For 40 years, despite improvements in imaging, surgical technique, and the delivery of radiation therapy, survival has remained the same. Recent reports show promise after years of stagnation. Despite these recent advances, several areas, such as the optimal chemotherapy regimen and dose escalation in radiation therapy, should be actively investigated.


   ACKNOWLEDGMENT
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The authors wish to thank Julian Thomas for proofreading the manuscript.


   REFERENCES
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 Learning Objectives
 Abstract
 History
 Diagnosis and Work-up
 Treatment
 Current Recommendations and...
 Summary
 References
 

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Received January 27, 2004; accepted for publication May 10, 2004.





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