Primary Malignant Lymphoma of the Parotid Gland

ORIGINAL ARTICLE Primary Malignant Lymphoma of the Parotid Gland

Leon Barnes, MD; Eugene N. Myers, MD; Emanuel P. Prokopakis, MD

Objectives: To document the clinicopathologic fea- mas were staged and treated with local irradiation and/or tures of primary malignant lymphoma of the parotid gland chemotherapy. based on analysis of our cases and to compare the results with similar studies in the literature. Results: Fifteen men and 18 women aged 26 to 100 years (mean, 66 years) had an enlarging painless mass on ini- Design: Retrospective, nonrandomized case study. tial examination. Seven (21%) had an underlying autoimmune disease and 20 (61%) had Ann Arbor stage I dis- Setting: Academic, tertiary medical center. ease at diagnosis. Of 25 patients available for a minimum 2-year follow-up, 16 (64%) were alive with or without Patients: Forty-one consecutive cases of malignant disease. Histological grade was the only prognostic fea- lymphomas of the parotid gland were identified ture associated with outcome (PϽ.01). among 820 patients who had undergone parotid surgery during the course of 22 years. Thirty-three (80%) Conclusions: Our study, when viewed collectively with of these were primary lymphomas and were included those in the literature, indicates that malignant lympho- in the study. Eight (20%) occurred in patients with a mas of the parotid gland are uncommon and often not history of malignant lymphoma and were therefore suspected clinically. The disease affects both sexes equally excluded. and is unusual before the age of 50 years. Most are B- cell, non-Hodgkin lymphomas, and about 80% of pa- Intervention: Diagnosis was established by open patients have Ann Arbor stage I or II disease at diagnosis. rotid biopsy in 8 patients, superficial lobectomy in 23, and total parotidectomy in 2. After diagnosis, lympho- Arch Otolaryngol Head Neck Surg. 1998;124:573-577

RIMARY malignant lympho- Twenty-four patients (73%) were be- mas of the salivary glands are tween 50 and 80 years of age, while only uncommon, comprising only 4 (12%) were younger than 50 years. 1.7% to 3.1% of all salivary The most common clinical manifes- neoplasms1-3 and 0.6% to 5% tation was a progressively enlarging, non- of all tumors and/or tumorlike lesions of the fixed mass that was painless in 30 pa- P 1,4-8 parotid gland. Although the parotid gland tients (91%) and painful in 3 others (9%). is by far the most common site of origin, ma- Only 3 patients (9%) had coexistent en- lignant lymphomas may also involve, in de- larged cervical lymph nodes. Five pa- scending order of frequency, the subman- tients (15%) exhibited facial nerve pare- dibular gland, minor salivary glands, and sis, but of these, only 1 complained of pain. sublingual gland (Table 1).2,3,9-13 The stage of disease was I in 20 pa- In the parotid gland, malignant lym- tients (61%), II in 7 (21%), III in 2 (6%), phomas are often clinically unsuspected, and IV in 4 (12%) (Table 2). Seven pa- manifesting as nonspecific masses indis- tients (21%) had a history of an autoim- tinguishable from other more common epi- mune disease (Sjo¨gren syndrome in 5 and thelial tumors. We therefore decided to rheumatoid arthritis in 2), and at least 3 review our experience with parotid lym- (11%) of 28 patients had other coexist- phomas during a span of 22 years to see ent malignant neoplasms (squamous cell if they exhibited a characteristic clinico- carcinoma of the lung in 1, adenocarci- pathologic profile and, if so, whether there noma of the breast in 1, and adenocarci- were any clinical features that might sug- noma of the colon in 1). From the Departments of gest the diagnosis before surgery. Pathology (Dr Barnes) and PATHOLOGIC FINDINGS Otolaryngology (Dr Myers), University of Pittsburgh School RESULTS of Medicine, Pittsburgh, Pa; and Although some of our cases predated the Department of Otolaryngology, CLINICAL FINDINGS immunohistochemical era, the diagnosis University of Crete School of of malignant lymphoma was confirmed in Medicine, Crete, Greece There were 15 men and 18 women with a 28 of the 33 cases in which the slides were (Dr Prokopakis). mean age of 66 years (range, 26-100 years). available for review. The remaining 5 cases

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PATIENTS AND METHODS The diagnosis of malignant lymphoma of the parotid gland was established by open biopsy in 8 patients (24%), su- A retrospective review of the clinical records and ana- perficial lobectomy in 23 (70%), and total parotidec- tomical pathology files of the Eye and Ear Institute tomy in 2 (6%). Five patients who underwent superfi- and the University of Pittsburgh Medical Center, Pitts- cial lobectomy also had a cervical lymph node biopsy. burgh, Pa, from September 1, 1972, through Octo- Three patients had a fine-needle aspiration of their ber 31, 1994, disclosed 820 patients who had under- salivary tumor before surgery; of these, 2 specimens were gone surgery of the parotid gland for the presence of interpreted as benign and 1 as probably malignant. Seven a tumor or tumorlike mass. Of these, 542 patients (21%) of 33 patients had a frozen section performed; of (66%) had benign lesions and 278 (34%) had malig- these, 5 were interpreted as malignant and 2 as possibly nant lesions. Forty-one (5%) of the 820 cases were malignant. malignant lymphomas and, of these, 8 were from pa- After diagnosis, the patients were referred to an on- tients who had a history of malignant lymphoma and were therefore excluded. The remaining 33 cases were cologist for staging and treatment. Staging during the 22- considered to be primary lymphomas and are the sub- year time interval varied according to existing medical ject of this study. dogma and technology, but it generally included a thor- The medical records of these 33 patients were ough history and physical examination, complete blood reviewed for the following features: age, sex, initial cell count with bone marrow aspirate and biopsy, liver symptoms, physical findings, extent of surgical pro- function tests (usually total bilirubin, alkaline phospha- cedure, stage of disease, and histological type of tase, aspartate aminotransferase, and alanine aminotrans- lymphoma. The Ann Arbor system (Table 2) was ferase), and computed tomography of the chest, abdo- used for staging and the Working Formulation was 14,15 men, and pelvis. A few patients had lymphangiograms used for histological classification (Table 3). and random needle biopsies of the liver, but none un- Cases that did not conform to the Working Formu- lation were reviewed by one of us (L.B.) and reclas- derwent staging laparotomies. sified accordingly. Specific details of therapy were not always avail- Follow-up was obtained from medical records, able and, moreover, are beyond the scope of this article. from a tumor registry, or by letter or telephone con- In general, patients with localized disease were treated tact with the attending physician, patient, or family with postoperative radiation, while those with multifo- member. Data were analyzed statistically by ␹2 and cal or systemic disease received chemotherapy. 2-tailed Fisher exact tests when appropriate, with a A minimum 2-year follow-up was available in 25 of level of significance of PϽ.05. Multiple logistic re- the 33 patients (Table 4). gression of variables and Spearman rank correlation were also performed. STATISTICAL ANALYSIS

Statistical evaluation of selected variables showed that only histological grade (high vs intermediate and low) of the had been thoroughly evaluated by appropriate immuno- Working Formulation was clinically significant (PϽ.01); histochemical stains, and the stated diagnosis was the higher the grade, the worse the prognosis. Stage (I therefore accepted. The lymphomas were all of the non- vs II, III, and IV) almost achieved significance (PϽ.07). Hodgkin type and included 8 variants, the most com- Sex (PϽ.14), age at onset (PϽ.86), presence of an auto- mon of which was the follicular, small cleaved lym- immune disorder (PϽ.59), and specific histological type phoma, which accounted for 14 (42%) of the cases of lymphoma (PϽ.39) were not important prognostic (Table 3). Sixteen tumors were nodular (follicular) and variables. 17 were diffuse. Twenty (61%) of the lymphomas were low grade according to the Working Formulation, 15% were intermediate grade, and 24% were high grade COMMENT (Table 3). Of 28 cases in which the slides were available for A mass in the parotid gland may be the first manifesta- examination, the lymphoma was confined to the paren- tion of malignant lymphoma or it may represent a sec- chyma of the parotid gland in 17 (61%), and in 1 of ondary focus of disease in a patient with a known his- these the cervical lymph nodes were also affected. Seven tory of malignant lymphoma. In our series of 41 parotid lymphomas (25%) involved only the intraparotid lymphomas, 33 (80%) were primary and 8 (20%) were lymph nodes, and in 1 of these the cervical lymph secondary. These statistics on the frequency of primary nodes were also diseased. Four cases (14%) involved and secondary malignant lymphomas, however, may be both the parenchyma and intraglandular lymph nodes, misleading, since the occurrence of a parotid mass in a and in 1 of these the cervical lymph nodes were also patient with a history of malignant lymphoma is often involved. assumed to be lymphomatous and, therefore, not ex- Three (11%) of the 28 cases also showed histologi- cised for pathological evaluation. cal evidence of “benign lymphoepithelial lesion”; all 3 The majority (84%-97%) of all parotid lymphomas of these were from patients with clinical evidence of Sjo¨- are of the non-Hodgkin type and of B-cell origin, either gren syndrome. nodular or diffuse.2,3,10,12,16,17 Only 3% to 16% are caused

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Location, No. (%)

Source Total Parotid Submandibular Sublingual Minor Glands Gleeson et al2 30 21 (70) 5 (17) 1 (3) 3 (10) Schusterman et al3 25 19 (76) 6 (24) 0 (0) 0 (0) Freedman9 10 8 (80) 2 (20) 0 (0) 0 (0) Hyman and Wolff10 33 30 (91) 3 (9) 0 (0) 0 (0) Colby and Dorfman11 59 42 (71) 14 (24) 2 (3) 1 (2) Schmid et al12 25 21 (84) 4 (16) 0 (0) 0 (0) Takahashi et al13 15 14 (93) 1 (7) 0 (0) 0 (0) Total 197 (100.0) 155 (78.7) 35 (17.8) 3 (1.5) 4 (2.0)

Table 2. Ann Arbor Staging of 33 Malignant Table 3. Distribution of 33 Malignant Lymphomas Lymphomas of the Parotid Gland of the Parotid Gland According to the Working Formulation Classification Stage Description No. (%) I Involvement of single lymph node region (I) or single 20 (61) Grade No. (%) extralymphatic organ or site (IE) 1. Low grade 20 (61) II Involvement of Ն2 lymph node regions on the same 7 (21) A. Diffuse, small lymphocytic 4 side of the diaphragm (II) or localized involvement B. Follicular, small cleaved 14 of extralymphatic organ or site and Ն1 lymph node C. Follicular, mixed small cleaved and large cell 2 region on same side of diaphragm (IIE) 2. Intermediate grade 5 (15) III Involvement of lymph node regions on both sides 2 (6) D. Follicular, large cell 0 of diaphragm (III), which may also be accompanied E. Diffuse, small cleaved 1 by localized involvement of extralymphatic organ F. Diffuse, mixed small and large cell 2 or site (IIIE) or by involvement of the spleen (IIIS) G. Diffuse, large cell cleaved or noncleaved 2 or both (IIISE) 3. High grade 8 (24) IV Diffuse or disseminated involvement of Ն1 4 (12) H. Large cell immunoblastic plasmacytoid 7 extralymphatic organ or tissue with or without I. Lymphoblastic 0 associated lymph node enlargement; reason for classifying as stage IV should be identified further by J. Diffuse, small noncleaved/Burkitt 1 defining site by symbols: H+, liver involvement; L+, 4. Miscellaneous 0 (0) lung involvement; M+, marrow involvement; P+, K. Composite 0 pleural involvement; D+, skin involvement L. Mycosis fungoides 0 M. Other 0 Total 33 (100)

Table 4. Survival Data of 25 Patients in Current Series frequently are associated with a “benign lymphoepithe- With a Follow-up of 2 Years or More lial lesion,” and are often curable.18-25 A few, however, may disseminate to lymph nodes or other MALT sites or Status No. (%) even transform to a higher-grade lymphoma.26 Alive, no evidence of disease 11 (44) One of the deficiencies of the Working Formula- Alive with disease 5 (20) tion classification of malignant lymphomas is that it does Dead of disease 4 (16) Dead of other cause 5 (20) not contain a specific category for MALT lymphomas Total 25 (100) (Table 3). Since MALT lymphomas may have a range of cellular sizes, they are often spread among several cat- egories of the Working Formulation, including small lym- by Hodgkin disease and, while T-cell lymphomas have phocytic, small cleaved, and mixed small and large cell.22 been described, they are exceptional.17 The new Revised European-American Lymphoma (REAL) The lymphoma may arise in intraglandular lymph classification, however, does take MALT lymphomas into nodes normally found in the parotid gland or from the consideration.27,28 parenchyma (mucosa-associated lymphoid tissue There is considerable confusion in the literature on [MALT]) or both. In our study, of the 28 cases in which the use of the terms primary and secondary, and nodal slides were available for examination, 7 (25%) of the lym- and extranodal, in regard to malignant lymphomas of the phomas arose in intraparotid lymph nodes, 17 (61%) from parotid gland.2,29,30 We use the term primary for any ma- the parenchyma, and 4 (14%) from both sites. lignant lymphoma that first manifests in the parotid gland, The distinction of nodal vs parenchymal (MALT) regardless of the subsequent stage of the disease, whether origin of a salivary lymphoma has some clinical signifi- it arises in the parenchyma or intraglandular lymph nodes, cance, since many of the parenchymal (MALT) lympho- or whether it is associated with an autoimmune disor- mas tend to be low grade, are localized at the time of di- der. When a parotid lymphoma develops in a patient with agnosis and often remain so for extended periods, a known history of malignant lymphoma, we arbitrarily

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©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 Table 5. Ann Arbor Stage of 110 Malignant Table 6. Working Formulation Classification of 124 Lymphomas of the Parotid Gland Malignant Lymphomas of the Parotid Gland

Stage, No. (%) Grade, No. (%)

Source Total I II III IV Source Total Low Intermediate High Gleeson et al2 30 19 7 2 2 Gleeson et al2 46 33 13 0 Mehle et al8 16 5524 Watkin et al7* 14 770 Schmid et al12 21 91200 Mehle et al8 16 853 Liang and Loke33 10 3205 Takahashi13 15 3102 Present series 33 20 7 2 4 Present series 33 20 5 8 Total 110 (100.0) 56 (50.9) 33 (30.0) 6 (5.5) 15 (13.6) Total† 124 (100.0) 71 (57.3) 40 (32.3) 13 (10.5)

*Initially diagnosed by the British National Lymphoma Investigation Classification and reclassified by us according to the working formulation. designate it as secondary. Others use the term primary †Percentages may not equal 100 due to rounding. only when the lymphoma originates in the parenchyma (MALT) as opposed to intraparotid lymph nodes. Still ing skin or deep tissues.2,3,7 The incidence of finding an others apply the term primary only when the lymphoma underlying coexistent autoimmune disorder, such as Sjo¨- appears de novo and secondary when it is associated with gren syndrome and rheumatoid arthritis, has ranged from an underlying autoimmune disorder, such as Sjo¨gren 0% to 44%.2,8-10,13,33 syndrome. While some investigators distinguish nodal At the time of diagnosis, most patients are found to from parenchymal lymphomas, others consider all have Ann Arbor stage I (51%) or II (30%) disease and parotid lymphomas, regardless of site of origin, as low-grade (52%) to intermediate-grade (37%) malig- extranodal and indicate that they constitute about 8% of nant lymphomas according to the Working Formula- all extranodal lymphomas of the head and neck.31,32 tion (Table 5 and Table 6). These inconsistencies in terminology and the ever- Our review indicates that primary malignant lym- changing histological classification of malignant lymphoma of the parotid gland is rarely suspected preop- phomas make comparison of various studies on salivary eratively. The following clinical features might suggest lymphomas difficult. the diagnosis: development of a parotid mass in a pa- Some investigators have noticed a progressive in- tient with a known history of malignant lymphoma; oc- crease in the incidence of salivary lymphomas during the currence of a parotid mass in a patient with an immune last several decades.3,16 This may result from a combina- disorder, such as Sjo¨gren syndrome, rheumatoid arthri- tion of factors: (1) referral patterns, (2) increased life span tis, or acquired immunodeficiency syndrome; occur- of individuals who are at risk for developing the disease, rence of a parotid mass in a patient with a previous di- and (3) the realization that with the use of sophisticated agnosis of “benign lymphoepithelial lesion”; multiple molecular techniques, many of the “benign lymphoepi- masses in a unilateral parotid gland or bilateral parotid thelial lesions” are actually subtle examples of lym- masses; or parotid mass associated with multiple, en- phoid malignant neoplasms. larged unilateral or bilateral cervical lymph nodes. Malignant lymphomas of the parotid gland are un- Our approach to any salivary mass, even those sus- common in patients younger than 50 years. The peak age pected of being a primary malignant lymphoma, is ex- of occurrence is between 50 and 80 years, with a mean cision. In the case of the parotid gland, this usually en- or median age in most series of 55 to 65 years (range, tails a superficial lobectomy. The rationale of this approach 20-100 years).2,3,7-13,22 Although various studies have in- is as follows: (1) A variety of epithelial salivary tumors dicated a male-female ratio varying from 2:1 to 1:1 to 1:2, either contain or are often associated with an exuberant our collective review of 269 cases, including 33 in the lymphoid element, such as the Warthin tumor, seba- current series, shows the sex distribution to be about ceous lymphadenoma, lymphoepithelial carcinoma, and equal: 125 men (46%) and 144 women (54%).2,3,7-13,33 acinic cell carcinoma.34 On small biopsy specimens, these Most patients with malignant lymphomas of the pa- tumors may be confused with malignant lymphomas or rotid gland show a progressively enlarging, unilateral, result in an uncertain diagnosis. (2) Malignant lympho- painless mass of 0.5 to 8.0 cm in greatest dimension as- mas developing in a background of “benign lymphoepi- sociated with enlarged cervical lymph nodes in any- thelial lesion” may initially be focal and subtle and eas- where from 9% to 69% of cases.2,3,7,11,33 Although bilat- ily missed on a small biopsy specimen. (3) Excisional eral parotid lymphomas have been described in 4% to 21% biopsy also provides enough tissue for thorough rou- of patients, it is not always clear whether these patients tine histological evaluation and for additional special- actually have bilateral disease or whether they have a uni- ized studies, such as T- and B-cell markers, flow cytom- lateral lymphoma associated with bilateral “benign lym- etry, and gene rearrangement. (4) Parotid masses, even phoepithelial lesion.” In rare instances, a patient may have in a patient with known malignant lymphoma, are not a simultaneous malignant lymphoma involving both the always lymphomatous. Some are epithelial in origin and parotid and submandibular glands.11 may be even more aggressive than the lymphoma. A su- Other unusual signs and symptoms that have been perficial parotid lobectomy in the hands of an experi- described are pain (9% in this series), facial nerve pare- enced head and neck surgeon is a low-risk procedure. sis (4% to 15%), and fixation of the mass to the overly- Concerns in the past about facial nerve damage, salivary

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©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 6. Nussbaum M, Cho HT, Som ML. Parotid space tumors of nonsalivary origin. Ann Table 7. Prognosis of Malignant Lymphomas Surg. 1976;183:10-12. of the Parotid Gland 7. Watkin GT, MacLennan KA, Hobsley M. Lymphomas presenting as lumps in the parotid region. Br J Surg. 1984;71:701-702. 8. Mehle MF, Kraus DH, Wood BG, Tubbs R, Tucker HM, Lavertu P. Lymphoma of Source No. of Cases Survival the parotid gland. Laryngoscope. 1993;103:17-21. 9. Freedman SI. Malignant lymphoma of the major salivary glands. Arch Otolaryn- Gleeson et al2 30 52% probability of surviving 5 y gol. 1971;93:123-127. Mehle et al8 16 69% alive at 68-mo mean follow-up 10. Hyman GA, Wolff M. Malignant lymphomas of the salivary glands: review of the Schmid et al12 21 83% probability of surviving 5 y literature and report of 33 new cases, including four cases associated with the and 40% at 10 y lymphoepithelial lesion. Am J Clin Pathol. 1976;65:421-438. Freeman et al35* 69 67% at 5 y and 21% at 10 y 11. Colby TV, Dorfman RF. Malignant lymphomas involving the salivary glands. Pathol Annu. 1979;14:307-324. Present series 25 64% alive with follow-up of Ն1y 12. Schmid U, Helbron D, Lennert K. Primary malignant lymphomas localized in salivary glands. Histopathology. 1982;6:673-687. *Includes malignant lymphomas from all salivary glands. 13. Takahashi H, Tsuda N, Tezuka F, Fujita S, Okabe H. Non-Hodgkin’s lymphoma of the major salivary gland: a morphologic and immunohistochemical study of 15 cases. J Oral Pathol Med. 1990;19:306-312. 14. Carbone PP, Kaplan HS, Musshoff K, Smithers DW, Tubiana M. Report of the fistula, and cosmetic deformities are no longer valid. Fine- committee on Hodgkin’s disease staging classification. Cancer Res. 1971;31: needle aspiration and incisional biopsies, however, may 1860-1861. have merit in the medically compromised patient who 15. Non-Hodgkin’s Lymphoma Pathologic Classification Project. National Cancer In- stitute sponsored study of classification of non-Hodgkin’s lymphomas: sum- is a poor operative risk. mary and description of a working formulation for clinical usage. Cancer. 1983; Once the diagnosis is established, the patient should 49:2112-2135. 16. Sciubba JJ, Auclair PL, Ellis GL. Malignant lymphomas. In: Ellis GL, Auclair PL, be referred to an oncologist for staging and appropriate Gnepp DR, eds. Surgical Pathology of the Salivary Glands. Philadelphia, Pa: WB treatment. As noted above, the inconsistencies in termi- Saunders Co; 1991:528-543. nology make comparison between studies difficult. With 17. Chan JKC, Tsang WYW, Hui P-K, Sin V-C, Siu LLP. T- and T/natural killer-cell lymphomas of the salivary gland: a clinicopathologic, immunohistochemical and this in mind, the prognoses from several reviews are shown molecular study of six cases. Hum Pathol. 1997;28:238-245. in Table 7.2,8,12,35 18. Azzopardi JG, Evans DJ. Malignant lymphoma of parotid associated with Miku- The impact of histological grade, stage of disease, licz disease (benign lymphoepithelial lesion). J Clin Pathol. 1971;24:744-752. 19. Hyjek E, Smith WJ, Isaacson PG. Primary B-cell lymphoma of salivary glands and presence or absence of an underlying autoimmune and its relationship to myoepithelial sialoadenitis. Hum Pathol. 1988;19: disease on clinical outcome is controversial.2,8,36,37 In our 766-776. 20. McCurley TL, Collins RD, Ball E, Collins RD. 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