Ann Thorac Surg 1995;60:217-222
© 1995 The Society of Thoracic Surgeons
Current Reviews
Primary Malignant Melanoma of the Esophagus
Axel W. Joob, MD,
G. Kenneth Haines, III, MD,
Merrill S. Kies, MD,
Thomas W. Shields, MD
Departments of Surgery, Pathology, and Medicine, Northwestern University Medical School, Chicago, Illinois
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Abstract
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Primary malignant melanoma of the esophagus is a rare disease. A case is reported and the newer diagnostic techniques of immunohistologic identification of the tumor by positive reaction to the HMB-45 antigen, as well as immunoscintigraphy with Technetium-99m–labeled melanoma monoclonal antigen for the demonstration of distant metastasis, is presented. A current review of the literature on this uncommon tumor is presented, and treatment options are discussed. A total esophagectomy remains the treatment of choice. Four long-term (>5 years) survivors after adequate surgical removal have been recorded in the literature.
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Introduction
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Primary malignant melanoma of the esophagus is an uncommon tumor and comprises only 0.1% to 0.2% of malignant esophageal lesions [1, 2]. Baur [3] reported the first example of this tumor in 1906. Initially, most investigators considered such lesions as metastatic from some other known or unknown primary site. In fact, this latter event, as noted by Eng and Schneider and their associates [4, 5], is of even greater rarity.
Allen and Spitz [6] in 1953 suggested that the major criteria for accepting a melanoma as arising in the esophagus were the presence of junctional changes in the mucosa adjacent to the tumor and a typical histologic pattern of a melanoma and melanin within the tumor cells. Although a case exhibiting these criteria had been described in detail by Garfinkle and Cahan [7] the previous year, doubt persisted as to the primary occurrence of a malignant melanoma in the esophagus that was not dispelled for all intents and purposes until De la Pava and associates [8] identified the presence of typical melanocytes in the esophageal mucosa in 4 of 100 normal esophagi at autopsy examination. This finding subsequently was confirmed in studies by Tateshi and Ohashi and their colleagues [9, 10], who reported an incidence of 8% for the presence of melanocytes in normal esophagi of Japanese subjects.
At present approximately 180 cases of primary esophageal melanoma have been reported. Sabanathan and associates [2] recorded 139 cases in 1989, and Taniyama and colleagues [11] added 9 additional Japanese cases in 1990 [12–19] although some of these cases were no doubt included, but not documented, in the report of Suzuki and Nagoyo [1]. Since these reports 25 more publications reporting 32 new cases have appeared in the literature [20–44]. The exact number of cases is difficult to determine because it is apparent that some of the cases have been referred to in more than one publication from the same institution [7, 31, 45, 46].
In more than half of the cases reported, the diagnosis was not definitively established until examination of the resected esophagus or at autopsy of the nonresected patients. With the development of specific immunohistochemical techniques for the identification of melanocytic tumors using the monoclonal antibody HMB-45 by Gown and colleagues [47] and other investigators [48, 49], a definitive pretreatment diagnosis is possible in patients with this unusual primary malignant esophageal tumor. The purpose of this communication is to present a case identified preoperatively by this immunohistochemical technique and to review the current status of the identification, evaluation, and treatment of primary malignant melanoma of the esophagus.
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Case Report
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The patient, a 60-year-old white man with a history of dysphagia and odyophagia for a 6-week period, was admitted to another hospital, where a barium swallow and esophagoscopy revealed a partially obstructing, ulcerated polypoid lesion of the upper third of the esophagus. Computed tomography of the neck, chest, and upper abdomen revealed an esophageal mass in the upper third of the esophagus beginning just below the level of the cricoid cartilage and extending distally to within 3 cm of the level of the aortic arch. No enlarged lymph nodes or evidence of metastatic disease was observed. An incidental enlargement of the left lobe of the thyroid was identified. Biopsy of the lesion initially was interpreted as an undifferentiated malignant epithelial tumor (squamous cell carcinoma?). There was some tumor reactivity to the HMB-45 antigen demonstrated on immunohistochemical study, and a final diagnosis of malignant melanoma was suggested.
The patient subsequently entered Northwestern Memorial Hospital for additional evaluation and treatment. Repeat biopsy of the tumor was performed with minimal bleeding. Immunohistochemical staining with the HMB-45 antigen showed marked reactivity within many of the tumor cells. Reactivity for S-100 antigen was positive but there was no reactivity to cytokeratin AE1/AE3. A histologic diagnosis of a primary malignant melanoma was made. A metastatic workup was negative.
On June 21, 1994, the patient underwent a total esophagectomy via a transhiatal approach and a high cervical esophagogastric anastomosis was carried out. There was no gross extension of the tumor beyond the esophageal wall. No enlarged lymph nodes were identified. The postoperative course was uneventful except for a short-lived cervical anastomotic leak. The patient was discharged on the 18th hospital day in good condition.
The pathologic report described a 6 x 4-cm lesion (Fig 1
) that infiltrated deeply into the muscularis propria but not beyond it on microscopic examination. The tumor was composed predominantly of plump, spindle-shaped cells (Fig 2). The proximal margin was free of tumor. There was lymphatic and vascular permeation by the tumor cells. Immunohistochemical studies confirmed the preoperative diagnosis of primary malignant melanoma of the esophagus (Fig 3).
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Fig 1. . Photograph of the gross specimen revealing a 6 x 4-cm ulcerated polypoid mass near the proximal margin of the esophagus.
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Fig 2. . Photomicrograph of the tumor revealing tumor composed predominantly of plump spindle-shaped cells. (Hematoxylin and eosin.)
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Fig 3. . (A) Photomicrograph of tumor with hematoxylin and eosin stain: melanoma cells with single prominent nucleus, pseudonuclear inclusions, and abundant eosinophilic cytoplasm are shown. (B) Tumor stained with immunoperoxidase stain: golden cytoplasmic staining within many of the tumor cells denotes immunoreactivity for the melanoma marker HMB-45.
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Incidence
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Mucosal melanomas according to Mills and Cooper [50] account for 3% of all melanomas in whites, whereas they account for more than 33% of all melanomas in Japanese, in whom the overall incidence of malignant melanoma is less frequent [51]. In the esophagus, as previously noted, primary malignant melanomas account for 0.1% to 0.2% of all malignant lesions in most populations. However, incidences of almost 0.4% were reported in series of esophageal malignancies from Finland and China, and in a report from Denmark the incidence was 0.5% [26, 52, 53].
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Clinical Features
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Primary malignant melanomas of the esophagus occur twice as frequently in men as in women [2]. However, in the Japanese this ratio is reduced, the reason for which remains unknown. The tumor most frequently occurs in the 6th and 7th decades, although this lesion has been described in a child as well as in young adults [32, 48, 54–56].
Symptomatology mimics that of any malignant obstructing lesion of the esophagus. Occasionally hematemesis and melena are observed. Physical findings other than evident weight loss generally are absent. Sabanathan and associates [2] did report a 7% incidence of palpable left supraclavicular lymph nodes, which were the result of metastatic involvement.
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Pathology
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Primary malignant melanomas of the esophagus are grossly polypoid and may vary greatly in size. The base may vary in extent as well. Superficial ulceration may be present but otherwise the tumor is covered by intact squamous cell mucosa. The tumor is most often solitary although multiple polypoid lesions have been recorded [23, 43, 57]. Multiple lesions must be differentiated from ``satellite'' nodules, which may be present in 12% of cases and which are usually close to but not necessarily adjacent to the primary tumor [2]. The tumors often are located in the middle and lower thirds of the esophagus, although infrequently they can be located in the upper third. According to Chalkiadakis and colleagues' review [58], 7% occurred in the upper esophagus, 7% in the upper to middle, 24% in the midesophagus, 22% from the middle to lower, and 40% in the lower esophagus. The tumor is most often grossly pigmented, but this finding may be absent in 10% to 25% of cases [2, 11, 50]. In patients with a typically pigmented melanoma the adjacent esophageal mucosa may show melanosis, either focal or diffuse, in approximately 25% of cases [2, 46, 59].
Occasionally, the lesion may be amelanotic grossly but melanin can be demonstrated histologically. A more strict definition is that melanin also should be absent on histologic examination for the tumor to be classified as an amelanotic melanoma, but this is not commonly adhered to in most reports. Using this criterion the incidence of a true amelanotic melanoma is less than 2% [36].
The histologic features of the tumors are the same as those observed in malignant melanomas elsewhere in the body. The overlying squamous epithelium is most often normal but may show junctional changes [46]. The adjacent mucosal areas more frequently exhibit junctional changes, and melanocytes also may be identified.
Di Costanzo and Urmacher [46], as well as Watanabe and colleagues [36], among others, have described the electron microscopic features of the tumor. Premelanosomes as well as fully developed melanosomes are readily identified.
The tumor tends to grow in the mucosal and submucosal layers in a lentiginous radial manner, but deeper infiltration into the muscular layers of the esophagus can occur [46]. Infiltration beyond the esophageal wall is uncommon. The tumor has a tendency for vertical growth within the esophageal wall. Lymphatic and vascular invasion is common.
Immunohistochemically these tumors react to S-100 protein, neuron-specific enolase, and HMB-45 antibody but not to cytokeratin or CEA [11, 45]. The HMB-45 reactivity is believed to be specific in its reaction to melanomas, junctional nevus cells, junctional component of compound nevi, Spitz nevi, blue nevi, dysplastic nevi, and fetal and neonatal melanocytes, but there is no reactivity to adult melanocytes [47, 48, 60, 61].
With immunohistochemical staining on standard light microscopic examination the deposition of the protein A-gold complex indicative of HMB-45 immunoreactivity appears to be diffuse in the cytoplasm [47]. However, Taatjes and colleagues [49] have reported that by immunoelectron microscopy the HMB-45 antibody reaction specifically stains the melanosomes.
The metastatic spread is both by lymphatic and vascular routes. Locoregional lymph node involvement is common, particularly involving the thoracic, celiac, and supraclavicular lymph nodes. Vascular dissemination is most common to the liver, lungs, pleura, peritoneum, brain, and bone in order of decreasing frequency, although no site is immune. Thirty percent to 40% of patients have lymph node or distant metastasis present at the time of diagnosis, and approximately 85% of the reported patients, regardless of treatment, die with disseminated disease [2].
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Diagnosis
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Once the patient presents with the history of an obstructing esophageal lesion, endoscopy and appropriate radiographs are obtained. Biopsy and subsequent appropriate immunohistochemical studies then may establish the diagnosis definitively.
Chest radiographs and barium swallow should be routine. As a rule the tumor on contrast barium esophagram will appear as a bulky polypoid intraluminal filling defect. Ulceration may or may not be detected. The chest radiograph may on occasion reveal a parenchymal mass suggesting a pulmonary metastasis. Computed tomography of the chest and upper abdomen may reveal the presence of the esophageal lesion and at times suggests the presence of lymph node, pulmonary, liver, or other abdominal involvement.
At endoscopy, the tumor is polypoid and the aforementioned gross pathologic features may be observed in varying combinations. The tumor is often friable and bleeds readily on manipulation and biopsy, but excessive bleeding is rare.
Cytologic smears are variably diagnostic of melanoma. Standard histologic examination is interpreted as diagnostic of a malignant melanoma in 54% of cases [2]. Junctional changes in the adjacent mucosa are present in approximately a third to one half of the cases. Specific immunohistochemical staining with the HMB-45 antibody should be carried out on all pigmented or even nonpigmented polypoid lesions of the esophagus. Positive reaction to HMB-45 antibody supports a diagnosis of malignant melanoma. Other immunohistochemical staining with neuron-specific enolase and S-100 protein may be done, but even when positive these studies are not diagnostic per se. The tumor is regularly negative for the presence of cytokeratin.
Evaluation for the presence of metastatic disease and locoregional lymph node metastases should be done in all cases by the appropriate multiple radionuclide or computed tomographic scans. Recently the use of immunoscintigraphy with indium-111–labeled monoclonal antibody for the detection of metastatic disease in patients with cutaneous malignant melanoma has been suggested by Murry and associates [62]. However, the use of technetium-99m–labeled melanoma monoclonal antigens appears to yield better and more complete identification of metastatic disease, with positive results in identifying up to 80% of all metastatic lesions [63–65]. In patients with metastases from a primary cutaneous melanoma Salk and the Multicenter Study Group [64] reported a multiinstitutional study in which the detection rate of identification by the use of 99mTc-labeled antibodies was 95% for bone lesions, 91% for those in the liver, 78% for lymph node metastases, 62% for those in the brain and spleen, and 58% for those in the lung. Lamki and co-workers [65] have noted that the technique cannot identify deposits 1 cm or less in size. They also reported that human antiglobulin against murine antibodies will develop in 40% to 70% of patients studied [65]. Chello and colleagues [42] reported the use of immunoscintigraphy for successful identification of multiple metastatic disease in a patient with primary malignant melanoma of the esophagus.
Despite the frequent involvement of the intrathoracic lymph nodes, the use of transesophageal ultrasonography for the identification of enlarged lymph nodes has been reported only once [29]. Because this finding alone would have little bearing on the choice of treatment, this diagnostic study is probably not necessary.
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Treatment Options
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The choice of therapy is primarily dependent on the functional status of the patient and the presence and extent of metastatic disease at the time of diagnosis. Surgical resection is the preferred method of treatment. Radiation therapy generally has been reserved for the patient with metastatic disease or a poor functional status. Laser resection as a method of palliation in patients with nonresectable disease has been recommended for both primary and metastatic malignant melanoma of the esophagus [5, 43, 66, 67] and appears to be successful in these situations. At present chemotherapy and immunotherapy have no major role in treatment, although numerous patients have received various regimens postoperatively.
Surgical resection should be contemplated for all patients either as a possibly curative but most likely as a palliative procedure. The presence of extensive metastatic disease or very poor functional status of the patient would negate this approach. When surgical resection is elected, a total or near-total esophagectomy should be carried out because of the tendency of the tumor to spread longitudinally. Whether the resection should be done by a modified Ivor-Lewis or a transhiatal technique as done in our patient is unanswered. Many believe that a radical lymphadenectomy should be accomplished, but there are no data to support its efficacy. Reconstruction of gastrointestinal continuity is best carried out by use of the stomach. Although the operative mortality in the various collected series ranges between 10% and 15%, at the present time a mortality rate of less than 5% should be achieved. The use of adjunctive irradiation generally has not been recommended.
Radiation therapy alone is a second choice, although effective palliation has resulted in some cases. It is primarily selected in patients who have excessive surgical risks, have significant metastatic disease at diagnosis, or refuse the surgical option.
Effective systemic treatment is needed but chemotherapy and immunotherapy have not been employed frequently. Dacarbazine (DTIC), nitrosoureas, and platinum analogues all have activity in cutaneous melanoma, and combination therapy often including tamoxifen is under study. Important biologic agents include interferons, interleukin-2, and adoptive immunotherapy. The published experience with esophageal melanoma is scant and the value of systemic therapy uncertain. Therefore, in patients who are not candidates for irradiation, supportive care only with possible laser resection of obstructing esophageal disease is the more acceptable option.
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Prognosis
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Sabanathan and associates [2] noted that the overall survival of patients with the disease is less than 1 year and only a third of the patients have survived longer than 1 year regardless of the mode of therapy. In an earlier review by Chalkiadakis and colleagues [58] the median survival was reported to be 13.4 months. After local (limited) surgical resection the average survival has been reported to be only 9 months but may be as short as 1.5 months [2, 50]. After radical resection the mean survival has been just greater than 14 months with some patients surviving 2 to 3 years. Almost all patients die of metastatic disease. There have been four 5-year survivals after resection (Table 1) [1, 35, 41, 68, 69]. One of these patients had regional lymph node involvement [35]. Thus approximately 2.2% of all patients with a primary malignant melanoma of the esophagus have been salvaged and remained alive beyond 5 years with adequate surgical therapy. For those patients treated by radical resection a long-term survival rate of slightly less than 5% can be extrapolated from the data in the literature.
Radiation therapy, undoubtedly due to the selection of the patients in whom it has been used, has resulted in an average survival of only 1.5 months [50]. However, one long-term survivor (51 months) has been recorded; the patient died of recurrent disease (see Table 1
) [70].
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Conclusion
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Primary malignant melanoma of the esophagus is a rapidly fatal disease. Long-term survival has been recorded in 4 surgical patients. In 3 the disease was apparently confined to the esophagus at the time of resection. The presence of lymphatic or blood-borne metastases, gross or occult, portends in almost all cases a fatal result. Prompt diagnosis by immunohistochemical monoclonal HMB-45 antibody staining should be carried out on all suspicious obstructing polypoid lesions of the esophagus, pigmented or not. Appropriate evaluation for the presence of metastatic disease may in the future be best carried out by immunoscintigraphy. The choice of therapy is most often extensive surgical resection of the esophagus even though in most patients it is only palliative in nature with the relief of the major complaints of dysphagia and other symptoms of obstructive esophageal disease. Radiation therapy or laser resection of the obstructing tumor may be successful temporarily in patients with advanced disease. A better understanding of the activity of available systemic therapy is needed.
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Footnotes
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Address reprint requests to Dr Joob, Department of Surgery, Northwestern University Medical School, 251 E Chicago Ave, Suite 1030, Chicago, IL 60611.
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Abstract
Introduction
