Mucoepidermoid Carcinoma of the Trachea ORIGINAL ARTICLES
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1 ORIGINAL ARTICLES Mucoepidermoid Carcinoma of the Trachea and Bronchus: The Case for Conservative Resection Robert H. Breyer, M.D., John R. Dainauskas, M.D., Robert J. Jensik, M.D., and L. Penfield Faber, M.D. ABSTRACT We report our experience with 5 patients with mucoepidermoid carcinoma treated by conservative resection, and review the literature on the 62 patients previously reported. A visual bronchoscopic diagnosis of adenoma was made in all 5 current patients. Bronchoscopic biopsy was performed in 4 and provided an accurate histological diagnosis in each. Conservative resection was accomplished with bronchoplastic techniques in 4 patients: sleeve lobectomy, 2; lobectomy with plastic bronchial closure, 1; and segmental tracheal resection, 1. The other patient underwent conventional lobectomy. All 5 patients are alive and free from disease 4 to 15 years following operation. The recently demonstrated correlation between histological grading and clinical behavior allows relatively benign variants of mucoepidermoid tumors to be accurately identified by bronchoscopic biopsy prior to thoracotomy. Because these tumors have a propensity to originate centrally in the tracheobronchial tree, bronchoplastic procedures frequently are required in order to accomplish tumor extirpation with limited pulmonary resection. Mucoepidermoid carcinoma arising in the tracheobronchial tree is an extremely rare tumor; the literature identifies only 62 previously reported cases. These neoplasms usually exhibit slow local growth without extending to regional lymph nodes and rarely metastasize to distant sites [2, 6, 11, 12, 181. Consequently, they are ideally suited for conservative resections. We have had experience with 5 patients with mucoepidermoid carcinoma of the tracheo- From the Departments of Cardiovascular-Thoracic Surgery and Pathology, Rush-Presbyterian-St. Luke s Medical Center, Chicago, IL. Accepted for publication June 19, Address reprint requests to Dr. Faber, Rush-Presbyterian-St. Luke s Medical Center, 1753 W Congress Pkwy, Chicago, IL bronchial tree. Bronchoplastic resections were accomplished in 4 and included sleeve lobectomy (2), lobectomy with plastic closure of the main bronchus (l), and segmental tracheal resection (1). The other patient underwent standard lobectomy. The case reports and a current review of the literature are presented. Case Reports Patient 1 A 20-year-old man was seen with massive hemoptysis. Mild, self-limited episodes of hemoptysis had occurred intermittently during the previous 18 months. Left lower lobe atelectasis was evident on the chest roentgenogram (Fig 1). Open tube bronchoscopy was performed on an urgent basis. The entire tracheobronchial tree was filled with blood and clots, but after irrigation, a tumor mass was seen occluding the orifice of the left lower lobe. Microscopic examination of a bronchoscopic biopsy specimen revealed low-grade mucoepidermoid carcinoma. At thoracotomy, complete atelectasis of the left lower lobe was present. Lobar and mediastinal lymph nodes were free from tumor on frozen-section examination. Left lower lobectomy was initially carried out by transecting the lower lobe bronchus close to the upper lobe bronchial orifice. Frozen section of the bronchial margin identified residual tumor cells. To avoid pneumonectomy and preserve lung tissue, a sleeve of bronchus was excised, making an anastomosis between the upper lobe and main bronchus (Fig 2). Frozen section verified that the bronchial margins were then free from tumor. Postoperative recovery was uneventful. Bronchoscopic removal of granulation tissue and suture material was required at infrequent intervals postoperatively. The patient is alive and well 58 months after operation by Robert H. Breyer
2 198 The Annals of Thoracic Surgery Vol 29 No 3 March 1980 Fig 1. (Patient 1.) Preoperative chest roentgenogram demonstrates left lower lobe atelectasis. Fig 3. (Patient 2.) Preoperative chest roentgenogram demonstrates right upper lobe atelectasis. Patient 2 A 44-year-old woman was seen with minimal hemoptysis of three weeks' duration. A similar episode had ceased spontaneously 8 months previously. She had been maintained on a regimen of orally administered anticoagulants since aortic valve replacement 2 years prior to this admission. Chest roentgenogram demon- Fig 2. (Patient 1.) Left bronchial tree: (A) final lines of bronchial division; (B) removal of the lower lobe; and (C) anastomosis of the upper lobe bronchus to the main bronchus. strated right upper lobe atelectasis (Fig 3). Flexible fiberoptic bronchoscopy revealed a round, polypoid tumor mass originating at the orifice of the right upper lobe bronchus. Bronchoscopic biopsy was obtained, and low-grade mucoepidermoid carcinoma was diagnosed on microscopic examination. The patient underwent a right thoracotomy on June 4, Mediastinal nodes were demonstrated to be free from tumor on frozensection analysis. Right upper lobectomy with bronchoplastic closure of the right main bronchus was accomplished (Fig 4). Frozen-section a M A C
3 199 Breyer et al: Mucoepidermoid Carcinoma ANTERIOR VIEW,,<~gi, Middle lobe Fig 4. (Patient 2.) Right bronchial tree: (A) final lines of bronchial division; (B) removal of specimen; and (C) plastic closure of the main bronchus. examination verified that the bronchial margin was free from tumor. The postoperative course was uneventful, and the patient is alive and well 54 months after operation. Patient 3 A 32-year-old woman who had had intermittent hemoptysis for 6 months and three episodes of pneumonitis over the past 3 years was admitted Fig 5. (Patient 3.) Right bronchial tree: (A) final lines of bronchial division; (B) removal of upper lobe and sleeve of main bronchus; and (C) anastomosis of the bronchus intermedius to the main bronchus. to our institution. Right upper lobe atelectasis was evident on chest roentgenogram. Flexible fiberoptic bronchoscopy revealed a 2 cm tumor, resembling an adenoma, in the right main bronchus at the orifice of the right upper lobe. Bronchoscopic biopsy demonstrated low-grade mucoepidermoid carcinoma. Right thoracotomy was performed on June 21, 1974, and exploration did not reveal any obvious lymph node involvement. Sleeve lobectomy of the right upper lobe was accomplished (Fig 5). Postoperative recovery was uneventful. The patient is alive and well 52 months after operation. Patient 4 A 14-Year-old boy was Seen by an allergist because of an 8-month history of wheezing re- ANTERIOR VIEW -4 C
4 200 The Annals of Thoracic Surgery Vol 29 No 3 March 1980 tube bronchoscopy revealed a 2.5 cm tumor at the orifice of the left lower lobe. Bronchoscopic biopsy demonstrated low-grade mucoepidermoid carcinoma. Left lower lobectomy was performed on April 14, Postoperative recovery was uneventful. The patient is alive and well 15 years after operation. Fig 6. (Patient 4.) Preoperative laminagram of the trachea clearly demonstrates an intratracheal mass. fractory to medical therapy. Routine chest roentgenogram suggested an intratracheal mass, which was clearly documented on laminagrams (Fig 6). Through a flexible fiberoptic bronchoscope, a tumor with the appearance of an adenoma was visualized 4 to 5 cm proximal to the carina. Biopsy of the lesion was not attempted because of the severely compromised airway. Resection was performed on December 22, 1974, through a midline cervical incision, which was extended through the sternum to the level of the second intercostal space. Segmental resection of the trachea with end-to-end anastomosis was accomplished without difficulty. Frozen-section examination verified the margins of resection to be free from tumor. Postoperative recovery was satisfactory. Hemoptysis on one occasion necessitated repeat bronchoscopy and removal of granulation tissue at the anastomosis. The patient is alive and well 48 months after operation. Patient 5 An 11-year-old boy was hospitalized because of an acute febrile illness and roentgenographic evidence of left lower lobe atelectasis. Open Pa tho logy Similar gross pathological findings were observed in all 5 patients. The tumors were all well circumscribed and polypoid, with an appearance resembling bronchial adenoma (Fig 7A). Microscopic examination revealed them to be composed of sheets of squamous cells admixed with vacuolated, mucus-producing cells (Fig 78). Some minor variations in histological detail were noted among the specimens: intercellular bridging was seen in one specimen (Patient 2), and intermediate cells were evident in another (Patient 4). The tumor extended through the bronchial wall and eroded cartilage in only 1 patient (see Fig 7B). However, in all specimens, mitoses were rarely seen, and nuclear pleomorphism or hyperchromatism was absent or present only to a minimal degree. Parabronchial lymph nodes were uniformly negative. Bronchoscopic biopsy specimens, obtained in 4 patients, demonstrated histological findings identical to those seen in the surgical specimens. Comment Each of the 5 patients was seen initially with a centrally located tumor producing symptoms of bronchial irritation or obstruction, including hemoptysis and recurrent infection. The 4 patients with bronchial tumors had roentgenographic evidence of lobar atelectasis. The central location of these neoplasms facilitated accurate bronchoscopic assessment. Biopsy of the 4 bronchial tumors was accomplished without complication. Although the well-circumscribed, polypoid appearance of the tumor in each instance grossly was thought to be that of bronchial adenoma, histological examination revealed low-grade mucoepidermoid carcinoma in each specimen. Conventional pulmonary resection for 3 central bronchial le-
5 201 Breyer et al: Mucoepidermoid Carcinoma B sults. This fact has prompted us to review the literature concerning this uncommon neoplasm in order to more accurately define the role of bronchoplastic resection in the treatment of tracheobronchial mucoepidermoid carcinoma. sions would have entailed pneumonectomy. In 1945, Stewart and co-workers [131 charachowever, with the application of bronchoplas- terized a previously unrecognized group of tic techniques, pneumonectomy was avoided salivary gland neoplasms and used the term successfully. The conservative resections in our mucoepidermoid tumor to describe them. Bron5 patients have provided excellent long-term re- chial tumors exhibiting histological details char- Fig 7. (Patient I.) (A) Low-grade mucoepidermoid carcinoma along a cartilage plate, which has erosion. (PAS; original magnification XZOO.) ( B ) Tumor composed of sheets of large squamous cells and pools of mucin. (PAS; original magnification X300.)
6 ~ ~~ 202 The Annals of Thoracic Surgery Vol 29 No 3 March 1980 Table I. Resection for Localized Mucoepidermoid Carcinoma Bronchoplasty or Sleeve Local Tumor Location Pneumonectomy Lobectomy Lobectomy Segment Resection Trachea Main bronchus Lobar bronchus Segmental bronchus Unknown Total acteristic of mucoepidermoid tumor were reported by Liebow [71 in 1952, and, on the basis of experience with 5 patients with such tumors, Sniffen and associates [121 in 1958 concluded that bronchial mucoepidermoid tumors were relatively benign neoplasms. Subsequently, isolated reports of highly malignant mucoepidermoid carcinoma of the tracheobronchial tree with widespread distant metastases and short survival did appear [3, 5, 91. More commonly, however, these tumors were described as slow growing, with little predilection for nodal or distant metastases [8, 10, 11, 17, 181. Reviewing the literature up to 1965, Reichle and Rosemond 1111 pointed out that no recurrence had been reported following complete resection of these tumors. They concluded that bronchial mucoepidermoid tumors appear to be benign, but did not rule out the possibility of malignant transformation. Since that review, an additional 38 patients with this tumor, including the 5 reported here, have been added to the literature [l, 2, 6, 14-16]. A current review of the reported patients with mucoepidermoid tumors of the tracheobronchial tree, including the 29 reviewed by Reichle and Rosemond [113 and the 38 subsequently reported, reveals that the tumors invariably originate in the trachea or proximal bronchus. Only 3 of 67 tumors were located distal to a lobar bronchus. Localized resectable disease was identified in 47 patients (70 /o), while in 17 patients (25'/0), either distant metastases were documented at the time of presentation or complete resection was not possible due to local mediastinal invasion. Informa- tion regarding the extent of disease was incomplete in 3 patients (5%). Three patients with localized disease did not undergo resection because of serious underlying problems 110, 121. An additional patient was diagnosed postmortem [91 and in a fifth patient, pathological examination revealed tumor in the margin of a tracheal resection [6]. This patient died of recurrent tumor following re-resection 28 months later. Complete resection of all disease was accomplished in the remaining 42 patients (Table 1). It is noted that for localized disease in the main or lobar bronchus, a pneumonectomy was done in 11 patients while a bronchoplastic procedure was accomplished in only 5. Overall, only 3 of the 42 patients treated by curative resection died of recurrent or metastatic tumor (Table 2). Two patients were lost to follow-up, and 2 died of unrelated disease at 1 month and 18 years postoperatively without tumor recurrence. Therefore, 35 patients remain free from disease after an average follow-up of 6.25 years (range, 9 months to 23 years). Results among the 17 patients who were seen with unresectable disease were uniformly fatal. Metastases to regional lymph nodes were rare in patients who underwent curative resections. Lymph nodes were free from tumor in 27 patients, and long-term survival includes 25 patients (93%). Only 1 of these patients subsequently was seen with recurrence, and this patient had had incomplete resection. Two patients had a positive nodal status. Multiple positive hilar nodes were found in the pneumonectomy specimen of 1 of them who died with distant metastases 3 months post-
7 203 Breyer et al: Mucoepidermoid Carcinoma Table 2. Extent of Disease, Treatment, and Results in 67 Reported Patients with Tracheobronchial Mucoepidermoid Carcinoma No. of Extent of Disease Patients Treatment No. of Patients Tumor-Related Mortality Localized 47 Nonoperative Inadequate resection Complete resection a Mediastinal invasion 17 Resection and irradiation andlor distant disease Nonoperative Unknown "Follow-up unavailable on 2 patients. operatively. The other patient with regional lymph node metastases was reported to be alive and well almost 2 years following sleeve lobectomy. The status of regional nodes is unknown in the remaining 13 patients. Two of them are alive, a long-term survival of 15%. The encouraging results in the 47 patients with localized disease reflect the low-grade malignancy typical of the majority of these neoplasms. Nevertheless, 17 of the patients were seen initially with incurable disease, and this factor confirms the existence of a highly malignant variant of this tumor. Histological grading has been utilized to predict clinical behavior of salivary gland mucoepidermoid tumors 141. These tumors are characterized by an admixture of mucus-producing and squamous elements and are histologically classified into low-grade (Grade I), intermediate (Grade 11), and highly malignant (Grade 111) types on the basis of cellular differentiation and activity. Recent reports demonstrate the prognostic value of histological grading in tracheobronchial mucoepidermoid carcinoma [2, 6, 15, 161. Leonardi and co-workers [61 reported longterm survival following resection in 6 patients with low-grade lesions, while 1 patient with a high-grade variant died at 38 months. Conlan and associates [21 reported curative resection and long-term survival in 4 patients with a Grade I tumor and in 2 of 3 patients with Grade I1 lesions. One patient with a Grade 111 histology was seen with distant metastases and died at 12 months. High-grade tumors were diagnosed in 12 patients reported by Turnbull and colleagues 115,161, and all died within less than 18 months. Due to their central location, tracheobronchial mucoepidermoid carcinomas are easily visualized at bronchoscopy. They generally are seen as circumscribed, polypoid tumors 12, 6, 101 and often are thought to be bronchial carcinoids or adenomas. Bronchoscopic biopsy has not been universally advocated, largely because of the theoretical risk of serious hemorrhage. We encountered no serious complications in our four biopsies, and biopsy has been safely performed by others 12, 101. Bronchoscopic biopsy prior to thoracotomy is valuable because of the demonstrated correlation between histological grade and clinical behavior. A biopsy diagnosis of low-grade mucoepidermoid carcinoma should alert the surgeon to expect a localized tumor without metastases that can be adequately treated by a planned conservative resection. A bronchoplastic or sleeve resection often will be required because of the propensity of this tumor to originate centrally in the tracheobronchial tree. Pneumonectomy was performed in 9 of the 42 patients reviewed in the literature who underwent complete resection (see Table 2). It is clear that such radical procedures are unnecessary for the low-grade mucoepidermoid carcinoma for which lobectomy or bronchoplastic resection is the procedure of choice. Mediastinal extension or lymph node invasion might dictate a more radical procedure for the rare, high-grade tumor seen without evidence of distant disease.
8 204 The Annals of Thoracic Surgery Vol 29 No 3 March 1980 References 1. Axelsson C, Bucharth F, Johansen A: Mucoepidermoid lung tumors. J Thorac Cardiovasc Surg 65:902, Conlan AA, Payne WS, Woolner LB, et al: Adenoid cystic carcinoma (cylindroma) and mucoepidermoid carcinoma of the bronchus: factors affecting survival. J Thorac Carciovasc Surg 76:369, Dowling MB, Miller RE, Johnson IM, et al: Mucoepidermoid tumors of the bronchi. Surgery 52:600, Healey WV, Perzin KH, Smith L: Mucoepidermoid carcinoma of salivary gland origin: a classification, clinical-pathologic correlation, and results of treatment. Cancer 26:368, Larson RE, Woolner LB, Payne WS: Mucoepidermoid tumor of the trachea. J Thorac Cardiovasc Surg 50:131, Leonardi HK, Jung-Legg Y, Legg MA, et al: Tracheobronchial mucoepidermoid carcinoma: clinicopathological features and results of treatment. J Thorac Cardiovasc Surg 76:431, Liebow AA: Tumors of the lower respiratory tract, in Atlas of Tumor Pathology. Subcommittee on Oncology of the Committee on Pathology of the National Research Council. Washington, DC, Armed Forces Institute of Pathology, 1952, section V, article 17, p Markel SF, Abell MR, Haight C, et al: Neoplasms of bronchus commonly designated as adenomas. Cancer 17:590, Ozlu C, Christopherson WM, Allen JD: Mucoepidermoid tumors of the bronchus. J Thorac Cardiovasc Surg 42:24, Payne WS, Ellis FH, Woolner LB, et al: The surgical treatment of cylindroma (adenoid cystic carcinoma) and muco-epidermoid tumors of the bronchus. J Thorac Cardiovasc Surg 38:709, Reichle FA, Rosemond GP: Mucoepidermoid tumors of the bronchus. J Thorac Cardiovasc Surg 51:443, Sniffen RC, Soutter L, Robbins LL: Mucoepidermoid tumors of the bronchus arising from surface epithelium. Am J Pathol 34:671, Stewart FW, Foote FW, Becker WF: Mucoepidermoid tumors of salivary glands. Ann Surg 122:820, Trentini GP, Palmieri B: Mucoepidermoid tumor of the trachea. Chest 62:336, Turnbull AD, Huvos AG, Goodner JT, et al: Mucoepidermoid tumors of bronchial glands. Cancer 28:539, Turnbull AD, Huvos AG, Goodner JT, et al: The malignant potential of bronchial adenoma. Ann Thorac Surg 14:453, Weiss L, Ingram M: Adenomatoid bronchial tumors: a consideration of the carcinoid tumors and the salivary tumors of the bronchial tree. Cancer 14:161, Wilkins EW Jr, Darling RC, Soutter L, et al: A continuing clinical survery of adenomas of the trachea and bronchus in a general hospital. J Thorac Cardiovasc Surg 46:279, 1963
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