THE NATURAL HISTORY OF TUMORS PECULIAR TO THE SALIVARY GLANDS
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1 THE NATURAL HISTORY OF TUMORS PECULIAR TO THE SALIVARY GLANDS FRANK VELLIOS, M.D., AND DALE DAVIDSON, M.D. Departments of Clinical Pathology and Surgery, Indiana University School of Medicine Tumors of the salivary glands because of their bizarre histologic appearances and relative infrequency continue to present problems in diagnosis pathologically. These neoplasms arise not only in the major salivary glands but also in accessory salivary gland tissue of the lips, palate, tongue and cheeks. These tumors were the subject of extensive studies by McFarland 7 who, after many years' experience with such lesions, believed that he was unable to distinguish histologically between benign and malignant neoplasms. Stewart, Foote and Becker helped clarify the classification of salivary gland neoplasms with their classical study of the mucoepidermoid tumors. Quattlebaum, Dockerty and Mayo 9 reviewed a group of cylindromas which they pointed out are adenocarcinomas with definite invasive and metastasizing propensities. These cylindromas have a long clinical course and have most frequently been confused with pleomorphic adenomas. Recent studies of salivary gland tumors by various groups have resulted in classifications of salivary gland tumors that are similar, variations in most instances being minor ones that reflect the types of cases seen in the particular study., - 4> 8 - " Further proof of the truly epithelial nature of mixed tumors by tissue culture methods has simplified the classification of these neoplasms. A review of the lesions of the major salivary glands and oral cavity studied in the Surgical Pathology Laboratory of the Indiana University Medical Center prior to July, 954, was undertaken in order to determine the relative frequency and the natural course of the various histologic types of salivary gland tumors. The cases were studied especially for evidence of multiple foci of origin, malignant change in a previously benign tumor and the appearance of metastases in cases with malignant tumor. The tumors were studied initially without benefit of history, and a classification similar to that proposed by others was evolved. There were 9 tumors of the salivary gland type in this series (Table ). In addition, whose exact histologic type was not determined and 6 tumors of supporting tissues were encountered in the parotid gland. An attempt was made to determine the present status of each patient and in 80 cases such information was obtained. On the basis of this study these tumors may be grouped as suggested by Byars and Ackerman as follows: (I) benign epithelial tumors () malignant epithelial tumors with a long clinical course; () malignant epithelial tumors with a rapid clinical course; (4) tumors occurring incidentally in the major salivary glands. Received for publication August 0, 954; accepted, November, 954. Dr. Vcllios is Assistant Professor of Clinical Pathology and Dr. Davidson is Assistant.Resident, Department of Surgery. 47 Downloaded from on 0 January 08
2 48 VELLIOS AND DAVIDSON Vol. 5 TABLE DISTRIBUTION OF SALIVARY GLAND TUMORS Parotid Submaxillary Sublingual Lip Palate Other, in Oral Cavity Total Benign epithelial tumors Pleomorphic adenoma Papillary cystadenoma lymphomatosum Intraductal papilloma Adenolymphoid lesion Slowly growing malignant epithelial tumors Malignant mixed tumor Cylindromatous carcinoma Low-grade mucoepidermoid carcinoma Malignant mucoepidermoid carcinoma Rapidly growing malignant epithelial tumors Epidermoid carcinoma Adenocarcinoma Undifferentiated carcinoma Totals Incidental tumors Neurofibroma Hemangioendothelioma Undiagnosed tumor Fibrosarcoma BENIGN EPITHELIAL TUMORS Pleomorphic adenoma or mixed tumor (myxochondrosarcoma, chrondroma, myxoma, adenoma). The mixed tumor of salivary gland origin has been given various names. Because we believe all of these tumors are adenomas, we prefer the term suggested by Willis of pleomorphic adenoma. There were 80 instances of this type of tumor in this series. This neoplasm is always encapsulated. The thickness of the capsule varies in different areas, and bosselation is frequent. The cut surface frequently has a glary mucoid appearance with areas resembling hyaline cartilage. Occasionally, cysts are present. There is no tendency for this tumor to invade surrounding structures, but extension of tumor into the capsule may be present. In our material we encountered no evidence of multicentric origin. Histologically, this tumor is characterized by the presence of tubes, or ducts, lined by small, uniform, cuboidal cells. These ducts usually contain an eosinophilic coagulum. They are frequently surrounded by small sheets of similar cells that at the periphery trail off into a mucoid stroma. The mucoid stroma is characteristic of almost all Downloaded from on 0 January 08
3 Feb. 955 TUMORS OF SALIVARY GLANDS 49 these tumors, and in nodules of recurrent tumor may be the only element seen in a given section. The cartilage-like areas (Fig. ) seen in mixed tumors almost always blend with mucoid zones, and no perichrondrium is present. In several instances the tumors were almost completely cellular, with only small foci of mucoid or cartilage-like areas present. In 4 cases, in the sections which were available, only epithelial areas were present. In areas of some of the mixed tumors other features may be noted. In our series these have included foci of squamous epithelium with formation of keratin pearls (Fig. ), collections of myoepithelial cells and foci of calcification and ossification. In instances there were areas resembling onkocytoma (oxyphil adenoma) (Fig. ), similar to that reported by others, 4 ' " although the remainder of the tumors were of the typical mixed-tumor type. There was no example of pure onkocytoma in our material. No tumor of the sebaceous gland of the adenoma type 0 was observed. These tumors were more common in female patients, 46 occurring in women and 4 in men. The ages of the patients ranged from 4 to 90 years, the majority being in the fourth to sixth decades. In 0 cases the patients noted their tumors more than 0 years before they sought therapy, but in most instances the duration was 5 years or less. The most common presenting symptom was that of a slowly growing tumor, but in several instances the patient complained of a rapidly growing mass. The size of the tumors ranged from to 8 cm. In 48 cases subsequent course of the patients is known for periods ranging from a few months to 4 years. Seventeen of these patients had recurrences. Eight of the latter group had their initial therapy at other institutions. Most of the recurrences appeared within years after initial surgery, but in some instances the patients waited many years before seeking further therapy. One patient developed 5 recurrences in a period of 5 years, but has now been symptomless for more than years. In none of the recurrences was there histologic evidence of a malignant change, and all of these patients have continued to have a benign clinical course. Papillary cystadenoma lymphomatosum (Warthin's tumor). The tumors of this type in our series occurred in the parotid gland. In instance the tumor was large, measuring 7 by 4.5 by 4 cm. The other tumors each measured about cm. All were encapsulated. The papillary projections were seen grossly in the largest tumor, and these were separated by coagulated secretions. Histologically, the tumors were composed of papillary projections (Fig. 4) lined by tall columnar, pseudociliated, eosinophilic cells with small round nuclei. In the largest tumor some regions showed metaplasia of the epithelium to stratified squamous type. The stroma of the papillary projections was occupied by numerous lymphocytes frequently forming follicles. These patients were men 5, 5 and 56 years old. The duration of the largest tumor was years. One of the other tumors had been present for 6 months. The presenting symptoms were those of a slowly growing mass in the parotid region. The patients have been followed for months, year and 9 years following excision without recurrence. Downloaded from on 0 January 08
4 50 VELLIOS AND DAVIDSON Vol. 5 Intraductal papilloma. There was case of intraductal papillary adenoma of the palate in this series. Histologically, the lesion was characterized by the presence of intracystic papillary projections (Fig. 5) similar to those seen in intraductal papillomas of the breast. No clinical data were available in this case. Benign lymphoepithelial lesion (Sjogren's syndrome, Mikulicz's disease, 8 sicca syndrome, adenolymphoma, lymphoepithelioma, adenoma lymphomatosum, lymphocytic tumor). There were instances of benign lymphoepithelial lesion 5 involving the parotid glands in our series. In both cases the disease was bilateral. Biopsies of the glands revealed encapsulated nodules of lymphoid tissue, the nodules resembling lobules of salivary gland. Within the lymphoid tissue there were tubules and islands of epithelial cells. These cells superficially resembled reticulum cells, but study elucidated their epithelial nature and their origin from ducts. In some areas there was partial or complete replacement of the epithelial islands by hyalinized connective tissue. We do not regard the lesion as neoplastic but include the cases here because they may be confused with tumors. Both of our patients were men, 9 and 7 years old. Peripheral blood counts in both instances were within normal limits. In the younger patient the masses in the parotid regions were associated with dryness of the mouth and eyes, and long bone and joint pain. In both instances the lesions, following biopsy, were treated with external radiation. There has been no recurrence after and years. MALIGNANT EPITHELIAL TUMORS WITH A LONG CLINICAL COURSE Malignant mixed tumor. AVe have classified case in this series as a malignant mixed tumor. Histologically, this tumor resembled the benign mixed tumors or pleomorphic adenomas, contained sheets of small epithelial cells (Fig. 6), mucoid and cartilaginous tissue, and the epithelial cells showed moderate variation and occasional mitoses. This patient first noted a mass in the parotid region at the age of years. Subsequently, there were attempts to excise it. In addition, he was treated at various times with external radiation that appeared to retard the growth. The tumor continued to invade locally, extending to the base of the skull. At the time of the patient's death, 5 years after onset, it was thought, on the basis of radiograms of the chest, that metastases were present in the lungs. No autopsy was performed, however. Cylindromatous carcinoma (cylindroma, basal-cell carcinoma with hyaline stroma, adenocystic carcinoma, adenoid cystic epithelioma, adenomyo-epithelioma). This type of carcinoma was seen in 7 cases and was primary in acessory salivary gland tissue as well as the parotid and submaxillary glands. The tumor was not encapsulated and had a great tendency to invade perineural lymphatics. Histologically, the tumor cells formed small plugs that were occasion- FIG. (left upper). Typical cartilage-like focus in a pleomorphic adenoma. X 75. FIG. (right, upper). Squamous metaplasia with a keratin pearl in a pleomorphic adenoma. X 75 FIG. (left lower). Area of typical onkocytes occurring in a pleomorphic adenoma. X 450. FIG. 4 (right lower). Papillary structure in a papillary cystadenoma lymphomatosum. Approximately X 50. Downloaded from on 0 January 08
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6 5 VELLIOS AND DAVIDSON Vol. 5 ally honeycombed. The cells were small, dark and relatively uniform. Mitoses were rare. The tumor cells were frequently embedded in a hyalinized stroma (Fig. 7), but in some areas the stroma showed a myxomatous change. This stromal change has led to confusion between these tumors and pleomorphic adenomas. In some instances the association of this tumor with salivary gland ducts may be detected in the sections. Seven of these tumors occurred in men and 0 in women. The ages of the patients varied from 8 to 8 years. In instance the tumor was found during a routine physical examination. The longest stated duration before initial therapy was 4 years, most patients seeking medical attention within years. The presenting symptom was usually that of a slowly growing mass although in several instances, in which the lesion was primary in the oral cavity, the patient entered complaining of an ulcer within the mouth. There were 0 patients who had been followed for more than years or who had developed recurrences. All were treated with surgery or radiation therapy, or both. In instances metastases to the lungs were present and of these patients also had evidence of intracranial metastases at the time of his death. Two patients have died with extensive local recurrences. Four patients are alive with persistent tumor locally for periods ranging up to years. Two patients are alive and free of disease clinically after and 4 years, respectively. Mucoepidermoid carcinoma. This type of carcinoma may be divided into a group with relatively low malignancy and a group with relatively high malignancy on histologic criteria, as suggested by Stewart, Foote and Becker. In both types both mucus-secreting epithelial cells and epidermoid cells are found although sometimes only with difficulty. Mucin may be readily demonstrated with the aid of the mucicarmine stain. The relatively benign group is locally invasive histologically and is justifiably classified as carcinoma. In this type, the tumor is generally composed of large cystic spaces lined in part by mucussecreting epithelium and in part by squamous epithelium (Fig. 8). The stroma is abundant so that the epithelial components of the tumor are widely separated. In the malignant form the stroma is relatively slight. The tumor cells form large sheets and usually the epidermoid pattern is readily apparent (Fig. 9). Cysts lined by mucus-secreting cells are usually small, but single cells containing mucin-filled vacuoles are present. Occasionally papillary projections are seen. Invasion of surrounding structures and perineural lymphatics and metastases to regional lymph nodes may be demonstrated. There were cases of the relatively benign form of mucoepidermoid carcinoma in this series, 4 in women, 6 in men and in the sex was not stated. The patients' ages ranged from 5 to 74 years, and the duration of symptoms before initial therapy, from months to year. All patients complained of a lump or "cyst" FIG. 5 (left upper). Intraductal papillary projections in a papillary adenoma of the palate. X 75. FIG. 6 (right upper). Myxoid and cellular area in a malignant mixed tumor of the parotid gland. X 50. FIG. 7 (lower). Plugs of epithelial cells arranged in cribriform pattern in a cylindromatous carcinoma. Foci of hyalinization within tumor are apparent. X 50. Downloaded from on 0 January 08
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8 54 VELLIOS AND DAVIDSON Vol. 5 in the involved area, and in this was associated with pain. Seven of these tumorsoccurred in the parotid gland and 4 in the oral cavity. Seven- of these patients have been followed years or longer. Two have developed extensive local recurrences and of these patients died with his disease- In other patient a recurrent lesion was excised but the patient is now free of disease, as are the other 4 patients. In none of the patients with this form of tumor have regional or distant metastases been demonstrated. Four patients with the malignant form of mucoepidermoid carcinoma hav& been seen. Three were women and a man; their ages were 8, 4, 58 and 74 years. All complained of a mass at the involved site. One patient was treated by local excision 5 years previously and has had no recurrence. The second patient also had excision of the mass from the parotid gland with dissection of the regional lymph nodes. Histologically, the lymph nodes revealed metastases of tumor and the patient has recurrent disease after year. The other patients have been, followed for only a few months. MALIGNANT EPITHELIAL TUMORS WITH RAPID CLINICAL COURSE This group includes epidermoid carcinoma ( case), adenocarcinoma ( cases) and undifferentiated carcinoma (5 cases) primary in the parotid gland (Fig. 0), and case of undifferentiated carcinoma of the sublingual gland. In all instances the tumor was removed locally and subsequently 5 were treated with external radiation. Seven of these 9 patients had distant metastases or have died with disease within periods of months to 6 years (average, ^ years). INCIDENTAL TUMORS Tumors of supporting tissues included hemangioendothelioma of infancy, neurofibromas and fibrosarcomas occurring in the parotid gland. Histologically and clinically they are similar to such lesions occurring in other sites. DISCUSSION Although tumors of the salivary glands assume diverse histologic forms, they are classifiable on histologic grounds. As suggested by Byars and Ackerman. these tumors may be divided into clinical groups depending upon their usual clinical course: () benign; () malignant with a long clinical course; () malignant with a rapid clinical course. The benign group includes about two thirds of the salivary gland neoplasms, mostly pleomorphic adenomas. Because of its bosselation the tumor may be cut across when excised so that recurrences have been frequent, especially when the surgeon was not familiar with its gross characteristics. In our series there has been no evidence of multicentric origin, and well-authenticated instances of such FIG. 8 (upper). Low-grade mucoepidermoid carcinoma. The layer of mucus-secreting cells in the upper portion of the field is part of the lining of a large cyst. X 0. FIG. 9 (left lower). Relatively malignant mucoepidermoid carcinoma. Many of the cells contain mucin droplets. Part of a cyst is seen in the upper portion of the field. Much of the tumor is composed of pavement epithelium. X 0. FIG. 0 (right lower). Undifferentiated carcinomaof sublingual gland. Mitoses are relatively frequent. X 40. Downloaded from on 0 January 08
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10 56 VELLIOS AND DAVIDSON Vol. 5 an occurrence are rare. It is difficult to prove that malignant tumors develop in benign pleomorphic adenomas but some suggestive evidence has been reported, such as sudden rapid growth in a previously slowly growing tumor, or areas resembling pleomorphic adenoma in an otherwise malignant lesion. The malignant tumors with a protracted clinical course include malignant mixed tumors, cylindromatous carcinoma and mucoepidermoid carcinoma. The true malignant mixed tumor is a relatively rare lesion accounting for less than per cent of all mixed tumors. It may perhaps result from a malignant transformation of the benign tumor. There was no histologic evidence for such a change in our case. This tumor is capable of metastasizing distantly as well as invading locally. The cylindromatous type of adenocarcinoma invades locally and along lymphatics, and metastasizes to regional lymph nodes and distantly. This type of tumor has a long clinical course even when distant metastases are evident. In of our cases the lesions in the lungs appeared to regress with radiation therapy and the patient remained active 8 months after lung metastases were first noted. Mucoepidermoid carcinoma also has a protracted clinical course. In our series, the "benign" form invaded locally but no lymph node or distant metastases developed. Metastases to regional lymph nodes were demonstrated in instance at the original operation for the "malignant" form of mucoepidermoid carcinoma. The malignant tumors with a rapid clinical course include adenocarcinoma, epidermoid carcinoma and undifferentiated carcinoma. These primary lesions are usually small when the patient first seeks medical advice. Metastases to regional lymph nodes and distant sites are the rule. Unfortunately, in most instances the true nature of the neoplasm is not appreciated until it is examined histologically. The role of the biopsy in surgery of neoplasms of the salivary gland should be appreciated. Histologic examination is the only method of ascertaining the benignancy or malignancy of salivary gland neoplasms. A properly planned initial surgical approach should enhance the "cure rate" of malignant salivary gland tumors. SUMMARY In a review of 9 salivary gland tumors 85 were classified as benign and 44 as malignant. These may be subdivided into various histologic types as suggested by many authors. For clinical purposes, they may be grouped into 4 categories:. Benign lesions: pleomorphic adenoma (mixed tumor), papillary cystadenoma lymphomatosum, intraductal papilloma, benign lymphoid lesions.. Malignant tumors with a slow clinical course: malignant mixed tumor, cylindromatous carcinoma, mucoepidermoid carcinoma.. Malignant tumors with a rapid clinical course: epidermoid carcinoma, adenocarcinoma, undifferentiated carcinoma. 4. Incidental tumors not peculiar to salivary glands. Downloaded from on 0 January 08
11 Feb. 955 TUMORS OF SALIVARY GLANDS 57 It is suggested that biopsy of the lesion be performed before therapy is undertaken in all persons with salivary gland tumors. Acknowledgment. We are indebted to Miss Dorothy Dickens, Registrar of the Tumor Registry, for her aid in obtaining follow-up data on many of the patients, and to Mr. James G. Glore and Mr. Paris Johnson of the Department of Illustration for preparation of the photographs. REFERENCES. BAUER, W. H., AND BAUER, J. D.: Classification of glandular tumors of salivary glands. Arch. Path., 55: 8-46, 95.. BUXTON, R. W., MAXWELL, J. H., AND FRENCH, A. J.: Surgical treatment of epithelial tumors of the parotid gland. Surg., Gynec. & Obst., 97: 40-46, 95.. BYARS, L. T., AND ACKERMAN, L. V.: Letter to the editor. J. A. M. A., 5: 54-55, FOOTE, F. W., AND FRAZELL, E. L.: Tumors of the major salivary glands. Cancer, 6: 065-, GODWIN, J. T.: Benign lymphoepithelial lesion of the parotid gland. Cancer, 5: 0S9-0, KIRKLIN, J. W., MCDONALD, J. R., HARRINGTON, S. W., AND NEW, G. B.: Parotid tumors: Histopathology, clinical behavior, and end results. Surg., Gvnec. & Obst., 9: 7-7, MCFARLAND, J.: The mysterious mixed tumors of the salivary glands. Surg., Gynec. & Obst., 76: -4, MORGAN, W. S., AND CASTLEMAN. B.: A clinicopathologic study of "Mikulicz's Disease." Am. J. Path., 9: 47-50, QUATTLEBAUM, F. W., DOCKERTV, M. B., AND MAYO, C. W.: Adenocarcinoma, cylindroma type, of the parotid gland. Surg., Gynec. & Obst., 8: 4-46, RAWSON, A. J., AND HORN, R. C: Sebaceous glands and sebaceous gland-containing tumors of the parotid salivary gland. Surgery, 7: 9-0, RAWSON, A. J., HOWARD, J. M., ROYSTER, H. P., AND HORN, R. C.: Tumors of the salivary glands. Cancer, : , STEWART, F. W., FOOTE, F. W., AND BECKER, W. F.: Mucoepidermoid tumors of salivary glands. Ann. Surg., : , WILLIS, R. A.: Pathology of Tumours. St. Louis: C. V. Mosby Co., 95, 997 pp. Downloaded from on 0 January 08
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