GUSENBAUE:R,
J Oral Maxillofac 48:409-415,
KATSIKERIS,
409
AND BROWN
Surg
1990
Primary Lymphoma of the Mandible: Report of a Case A.W. GUSENBAUER,
DDS,* N.F. KATSIKERIS, DDS, DR DENT,t AND A. BROWN, DDS, FRCD(C)$
Primary lymphoma of the mandible is rare, and misdiagnosis is common.’ Definitive diagnosis can be diffkult to establish even when a biopsy specimen is representative of the lesion and preparation of the material is optimal.’ Predominant radiographic features include rarefaction representing tumor osteolysis or secondary osteomyelitis,2 but these are not specific to this particular pathology. Pain, mobility, and destructive lytic lesions associated with the teeth may mimic endodontic or periodontal pathosis, leading to incorrect diagnosis and inappropriate treatment.3 A case referred to our service for diagnosis and treatment of an apparent chronic infection of the mandible following multiple dental extractions is presented. The difficulties involved in the diagnosis and treatment of this case involving primary mandibular lymphoma and osteomyelitis are highlighted. A review of primary lymphoma of the mandible, based on cases reported in the literature, is also presented. Report of a Case A 53-year-old white man was referred to an oral surgeon by his dentist for treatment of an apparent chronic infection in the anterior mandible. The six mandibular anterior teeth had been extracted several months previously. A panoramic radiograph revealed an osteolytic lesion in the anterior part of the mandible. The patient was subsequently admitted to Toronto General Hospital for investigation and treatment, with the provisional diagnosis of osteomyelitis of the anterior mandible.
* Resident, Oral and Maxillofacial Surgery, University of Toronto, Toronto, Ontario, Canada. t Clinical Instructor, Department of Oral and Maxillofacial Surgery, University of Toronto Faculty of Dentistry, Toronto, Ontario, Canada. $ Staff Surgeon, Oral and Maxillofacial Surgery, Toronto General Hospital, Toronto, Ontario, Canada. Address correspondence and reprint requests to Dr Gusenbauer: 790 Mohawk Rd W, No. 909 Hamilton, Ontario, Canada L9C 6C6. 0 1990 geons
American
Association
0278-2391190/4804-0015$3.00/O
of Oral
and Maxillofacial
Sur-
Medical history revealed that the patient had been a heavy cigarette smoker for 35 years. The patient had suffered a mild myocardial infarction in 1985, and had a previous history of stomach ulcer and kidney stones. Physical examination on admission revealed an obese man with positive findings related to the orofacial region, but otherwise normal findings. Minor tenderness to palpation was noted in the mental region, and further examination revealed apparent expansion of the anterior mandible both buccally and inferiorly (Fig 1). No abnormalities of the overlying mucosa were noted. The lower six anterior teeth were absent. No palpable lymph nodes were detected. Routine laboratory examinations were all within normal limits, with the exception of an erythrocyte sedimentation rate (ESR) of 19 (male reference, O-10). Electrocardiogram (ECG) showed minor ST-T segment changes. On chest radiograph, the heart and mediastinum were normal, lungs and pleura were clear, and bones were involved. Some osteolytic bone destruction was evident in the chin area on a lateral cephalogram taken on admission (Fig 2). Computed tomography (CT) examination of the mandible showed an osteolytic area in the anterior part of the mandible with destruction of some areas of buccal cortical bone (Fig 3). The patient was taken to the operating room for surgical exploration and biopsy under general anesthesia. Subperiosteal dissection in the mandibular anterior region revealed connective tissue adherent to a thin buccal cortex of bone which was necrotic in appearance from the region of the left first premolar to the right first premolar. This region was decorticated, and the bone and overlying soft tissue were submitted for histologic examination. Specimens were taken for aerobic and anaerobic cultures. Further exploration showed that the inferior border of the mandible and lingual cortex were intact. The surgical site was irrigated and packed with BIPP iodoform gauze for daily change while the patient was in the hospital. The patient was discharged on the second postoperative day and reappointed for dressing change and follow-up in the outpatient clinic the following week. A diagnosis of chronic osteomyelitis was given on the preliminary pathology report. The final pathology report, following en toto examination of the remaining tissue, suggested the possibility that some atypical cells seen in clumps in the marrow spaces may be representative of a lymphoproliferative disorder. Further investigations to rule out malignant lymphoma were advised. The biopsy procedure of the involved bone in the anterior region of the mandible was repeated on an outpatient basis, and a diagnosis of immunoblastic or diffuse large cell lymphoma of the mandible was made. The pa-
410
PRIMARY LYMPHOMA OF THE MANDIBLE
FIGURE 1. Swelling of mandible in chin region. FIGURE 3. Destruction of buccal cortex of bone is evident on CT scan. tient was subsequently readmitted to the hospital for staging and treatment planning. Laboratory values were again within normal limits excepting an ESR of 19. The chest radiograph and ECG were unchanged. Examination on admission now revealed an area of surface erythema over rhe skin of the mental region and visible enlargement of the area. The patient described a dull, intermittent, poorly localized pain, nonradiating in nature, as well as bilateral mental nerve paresthesia. The patient had also noticed a bad taste in his mouth, although ulceration and sinus tracts were not apparent. Bone marrow aspiration and biopsy of the iliac spine revealed no evidence of involvement by malignant lymphoma. On CT, no evidence of metastatic disease was noted. Hematologic consultation and subsequent staging revealed that the patient’s disease was limited to the anterior part of the mandible.
The patient was presented at Lymphoma Conference, at which time a diagnosis of malignant primary nonHodgkin’s lymphoma of the mandible, stage IE, diffuse large-cell variety with aggressive histologic pattern, was made (Fig 4). The recent presence of chronic osteomyelitis led to a decision to begin treatment with chemotherapy alone, with possible radiotherapy at a later date, to decrease the possibility of osteoradionecrosis. The patient’s chemotherapy was initiated in the hospital, and consisted of a course of cyclophosphamide, adriamycin and vincristin, plus prednisolone. On l-week follow-up the jaw size was almost normal and the tissue was noticeably softer. The patient was continued on the chemotherapy regimen for 3 weeks, and subsequently received externalbeam radiation therapy. At 9-month follow-up there was no evidence of residual tumor, no lymphadenopathy, and no evidence of progression of disease to other sites. A CT taken at l-year follow-up showed signs of healing of the original lesion. The patient remains free of disease at 18
months postsurgery. Discussion
FIGURE 2. Lateral cephalogram shows osteolytic lesion in anterior part of the mandible.
The features of primary lymphoma of the mandible are summarized from a review of series presented in the literature (Table 1). Although primary osseous lymphoma may account for up to 15% of all extranodal lymphomas,4 the mandible is an infrequent presenting site. Barkes noted that the average time between presentation and definitive treatment of oral lymphoma was 2.5 months and felt that the similarity of presentation of oral lymphoma to other common dental diseases was in part responsible for this delay. Mobility of teeth, pain, and osteolytic lesions associated with the teeth and jaws may mimic periodontal or endodontic pathosis, thus leading to an erroneous diagnosis and inappropriate treatment .3 A delay of several months between presentation of the pa-
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FIGURE 4. Histologic section showing large atypical cells and numerous mitotic ligures. (Hematoxylin-eosin stain. Original magnification, X240.)
tient to his dentist and referral to a specialist was noted in this case. Rarefaction in cases of malignant lymphoma of bone may represent tumor osteolysis or secondary Table 1.
osteomyelitis. The initial radiographic appearance of the present case was suggestive of osteomyelitis, and a similar appearance has been reported in severa1 such cases. On initial biopsy, osteomyelitis was
Primary Lymphoma of the Mandible: Reported Cases
Male/female Age (yr)
Campbell et al’
Eisenbud et al3
Eisenbud et al6
Robbins et al’
13/F 8-69
2/l 49
l/l 16
8/F 3-74
44
5
Macintyre”
l/l1 3/11 8111 l/l1 l/l1 IO/11
l/St l/St 4/5t
NS
19/21 12121 6121 6121 NS
213 l/3 l/3 l/3 l/3
212 l/2 212 l/2 l/2
Ill 1 6/ll 5/11 2111 NS
* Lesions may involve more than one anatomic location. t Results of 1984 and 1985 series combined.
Fukuda et al”
l/2 48
2/O 42
2/l 11
79
39
38
45
NS l/St 115t 4/5t
4116 3116 9/16 4116 4116 14/16
Slootweg et al”
l/l 52
29 Location* Ramus Angle Body Symphysis Anterior Posterior Stage I II III IV Clinical signs, symptoms Swelling Pain Numbness Loose teeth Lymphadenopathy
Howell et al”
Gusenbauer et al (this report) l/O 53
NS
212 l/l l/l 313 NS
212 l/2 o/2 o/2 012
313 l/3 l/3 NS NS
31/13 Avg 39.58 Median 42
51 NS
NS
Totals
1 1 0 0
NS NS NS NS NS
6132 II32 23134 II33 7142 35142 12124 4124 3124 5124
NS
NS NS NS NS
l/l O/l O/l 011 O/l
36143 22143 15143 1o/40 218
412
diagnosed and a suspicious clump of atypical cells was noted. The diagnosis, however, could not be made on initial biopsy. Robbins et al’ highlighted particular difficulty in diagnosis of primary lymphoma of the mandible. In a series of 11 patients, 5 patients could not be diagnosed on the basis of the initial biopsy. The investigators noted that all 5 patients requiring rebiopsy had lymphoma of the diffuse large-cell type. Our case required rebiopsy for definitive diagnosis and was also of the same histologic variety. The presence of concomitant osteomyelitis led to a modification of the usual combined therapy (chemotherapy and radiotherapy) in favor of chemotherapy alone in the initial phase of treatment to avoid possibility of osteoradionecrosis. Although extranoda! non-Hodgkin’s lymphoma (ENHL) of the head and neck area is common, the occurrence of malignant lymphoma of the oral cavity and pharynx is relatively rare.6 Aozosa et al7 found that oral malignant lymphoma (ML) represented 5% of a series of patients with ML of all varieties. In the series by Freeman et al* ML of the oral cavity comprised 2% of 1,467 patients with extranodal lymphoma. Takahashi et al9 reported that oral ENHL represented 8% of NHL and 37% of ENHL, whereas Barker’ stated that 20% to 34% of all ENHL occurs within the oral cavity when Waldeyer’s ring and the salivary glands are included. When considered in terms of total cases processed within oral pathology services, primary ENHL of the oral cavity represented only 0.2% and 0.1% of cases reported by Slootweg et al” and Tomich and Shafer, l1 respectively. The specific incidence of primary lymphoma arising in the mandible has not been addressed. Primary lymphoma of the mandible shows a 3 1: 13 male-female ratio, as summarized in Table 1. This is in agreement with Fukuda et al’s series of MLs of the oral cavity” (12:8 male-female ratio), although several other series of ML of the oral cavity report no significant sex predilection.10*‘3 Reported series of head and neck lymphomas have described both slight male predominance14*‘5 and slight female predominance. I6 The average age of presentation in the reviewed cases is 39.6 years, with a median age of 42 years. Peak incidence was in the 40- to 49-year age group, with 35% of cases occurring in the pre-30 age group and 35% in the post-50 age group. Series involving ML of the oral cavity have reported 60%” and 75%” of cases occurring in the over-50 age group. Howell et a1,l7 in reviewing the relationship between clinical features and the Lukes-Collins classification in 34 cases of extranodal oral lymphoma, found that patients with lymphoma composed of
PRIMARYLYMPHOMAOFTHEMANDIBLE
nontransformed follicular center cells had a greater mean age than those with tumors of transformed follicular cell centers or postfollicular cells. They also noted a trend of decreasing age of occurrence with increasing B cell transformation. The current review of primary lymphoma of the mandible did not contain sufficient cases classified according to the Lukes-Collins system to make this distinction. Mandibular lymphoma has been reported in the posterior part of the mandible in 37 cases, with only 7 cases involving the anterior portion of the mandible. Distribution by specific location within the mandible indicates that the body of the mandible is the most common location (23 cases), with the ramus angle and symphysis accounting for 6,7, and 8 cases, respectively. Numerous cases span these arbitrary anatomic divisions. Whereas the gastrointestinal (GI) tract is the major site of extranodal primary lymphomas,’ lymphoid aggregates which may undergo malignant transformation are also found in various head and neck locations. Within the oral cavity lymphoid aggregates are found in the floor of the mouth, lateral border and ventral surface of the tongue, buccal mucosa, tonsilar fauces, and hard and soft palate. Extranodal oral lymphoma may occur within soft tissue or bone. Fifteen per cent of Fukuda’s series occurred within bone,‘” as opposed to 35% in Howell’s series.17 Primary osseous lymphomas account for approximately 5% of all extranodal lymphomas.4 In the head and neck region, the maxilla is the most common site, and the mandible ranks second.” Within each of the LukesCollins classifications, the percentage of tumors that present with bony involvement appears to increase as the tumor category advances in B ceil transformation. l7 Swelling appears to be the most common presenting clinical finding in primary lymphoma of the mandible (84% of cases). Fukuda et alI2 also noted that a diffuse, painless swelling of the soft tissue was the initial presentation of most cases in his series of ML of the oral cavity. Pain was reported on initial clinical presentation in more than 50% of cases in the present review, whereas numbness (35%), loose teeth (25%), and cervical lymphadenopathy (12.5%) were less commonly reported clinical presentations. Hypoesthesia has been reported with or without radiographic evidence of involvement of the inferior alveolar canal. ’ Wang and Fleishil” noted that lymphoma occurring in osseous sites may extend into the medullary component or, in the case of the mandible, may involve the inferior alveolar canal, often without radiographic evidence of bony changes. The most common presentation of intraosseous lymphoma is rarefaction representing tumor osteolysis or sec-
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ondary osteomyelitis.2 Bony sclerosis at the periphery of the lesion has been reported in several reviews,’ whereas many cases present with a poorly defined diffuse margin without surrounding bone reaction.20 These features and a predilection for location in the premolar-molar region of the mandible are shared with intraosseous metastases.*’ Destruction of the lamina dura21 and pathologic fracture also have been described. Although resorption of tooth roots is not a common feature of intraosseous malignancies, isolated cases involving root resorption associated with lymphoma have been reported.‘*2’ Robbins et al’ noted one case involving the roots of a mandibular third molar in their series of primary lymphoma of the mandible. Other radiographic presentations noted in their series included diffuse osteolysis, focal osteolysis, widening of the mental foramen, and pathological fracture. In 2 of 11 cases there was no radiologic change. Slootweg et al” noted bony involvement in 16 of 20 cases of ENHL of the oral cavity, including several soft tissue cases exhibiting cortical erosion. They also noted that in 3 cases the initial radiographic appearance suggested periapical inflammation and had led to initial treatment consisting of extraction or periapical surgery. This appears to have been the presentation in our case as well. They also noted one mandibular lesion whose initial radiographic appearance had suggested osteomyelitis. A similar appearance was noted in the present case and osteomyelitis was, in fact, diagnosed on the original biopsy. Fukuda et al” noted destruction of neighboring bony structures in 4 of 11 malignant lymphomas of the gingiva. Table 2.
Definitive diagnosis of lymphoma may be difficult to establish even when optimal preparation of a representative specimen has been carried out.’ When nodal sites are involved, en toto excisional biopsy of involved nodes is preferred over incisional lymph node biopsy or needle biopsy in order to allow pathologic examination of the lymph node, capsule, and areas of normal and abnormal architecture side by side.22 Biopsy of the largest lymph node should be performed because surrounding nodes that may appear abnormal may simply show reactive hyperplasia.23 Extranodal lymphoma in the head and neck region may present a greater diagnostic challenge. This may be particularly evident when the disease is not suspected. 24 Interpretation of specimens from extranodal sites is also more difficult.’ Robbins et al’ discussed the necessity for removal of sufficient quantities of material in intraoral incisional biopsies to allow for histologic examination, including special stains, immunological studies for various surface markers, and electron microscopic investigation. Needle biopsy rarely provides sufficient material to fulfill these requirements. Areas to avoid on biopsy include previous biopsy sites with associated osteomyelitis, and other areas of inflammation. Superficial biopsies frequently identify only areas of chronic inflammation and necrosis.25 Based on the Ann Arbor Staging Classification,26 50% of cases of primary lymphoma of the mandible were classified as stage I (12/24 staged cases), 17% as stage II (4/24), 13% as stage III (3124)) and 21% as stage IV (5/24), on initial presentation. Considerable difficulty arises in summarizing the histopathologic findings of head and neck lymphomas due to
Histopathologic Classification of Reported Cases of Primary Lymphoma of the Mandible
Authot Eisenbud et al’
Rappaport Classification
NC1 Working Formulation
Lukes-Collins Classification
Diffuse histiocytic Diffuse, poorly differentiated lymphocytic Burkitt’s
2 2
Diffuse large cell Diffuse small cleaved
2 2
I
1
Eisenbud et al6
Diffuse lymphoblastic Burkitt’s
1 1
Slootweg et al’”
Diffuse mixed
1
Small noncleaved Burkitt’s Diffuse lymphoblastic Small noncleaved Burkitt’s Diffuse mixed small and large Diffuse large cell
Robbins et al’
Diffuse histiocytic Diffuse large cell Diffuse undifferentiated Burkitt’s Unclassified
1
1 1 1 1
7 2
1 I Diffuse small noncleaved Diffuse large noncleaved
Howell et al” Gusenbauer et al (this report)
Diffuse large cell
1
2
1
414 the number of different classification schemes used. Table 2 summarizes the histopathologic findings of reported cases of primary lymphoma of the mandible according to the NC1 Working Formulation,27 Rappaport Classification,28 or Lukes-Collins system.29 Within the NC1 classification, lymphoma of the diffuse large-cell type predominates. This appears to be consistent with series involving head and neck lymphomas,30-32 series involving the oral cavity in general,‘0,‘2 and also reflects the findings of Slootweg et al, lo who found that 8 of 14 cases of ENHL of the oral cavity arising specifically within bone were of the diffuse large-cell variety. By Rappaport classification, 3 of 9 cases arising within the mandible were classified as diffuse histiocytic. It appears that the relative predominance of this type is not confined to the mandible, the oral cavity, or the head and neck, but appears to be a feature of non-Hodgkin’s lymphoma (NHL) in general. lo Numerous series have shown a significant incidence of abdominal lesions as a first manifestation of progressive disease in patients with head and neck lymphoma. 3’ Takahashi et a1,9 based on autopsy findings, concluded that primary oral lymphoma spread via three modes: 1) lymphatic spread via cervical lymph nodes and intrathoracic and abdominal nodes to extranodal organs, 2) contiguous spread to adjacent organs, and 3) blood-borne distant metastases in late disease. The lung, kidneys, pancreas, liver, spleen, heart, GI tract, bone marrow, and adrenal glands were the most commonly involved viscera. This pattern of dissemination of primary ENHL of the oral cavity appears to behave like oral carcinoma with metastatic spread along primary drainage areas.31 Robbins et al’ noted spread of primary lymphoma of the mandible to cervical lymph nodes in 3 of 11 cases, pulmonary parenchyma in 1 of 11 cases, and liver in 1 of 11 cases. Although cervical lymphadenopathy was reported clinically in 12.5% of the cases presently reviewed, it is uncertain what proportion comprised reactive lymphadenopathy and what proportion represented true progression of disease. Various treatment regimens for head and neck lymphomas have been used and usually consist of irradiation, radiotherapy, surgery, or combinations of these. Most patients with NHL limited to the head and neck can be treated with radiotherapy with good results. Although chemotherapy is indicated in disseminated cases, recent trends at many centers is toward combined therapy for such cases, whereas surgery is generally reserved for excisable lesions.7 Conley et a130stated that combined therapy has been shown to offer the best prognosis in patients with intermediate- to high-grade histologic
PRIMARY LYMPHOMA OF THE MANDIBLE
types in a review of series of several investigators. Localized stage I and IE cases were treated with radiotherapy primarily, whereas patients with stage II to IV were treated with CHOP (cyclophosphamide, hydroxyldaunorubicin [doxorubicin], vincristine [oncovin], and prednisone) chemotherapy and irradiation. Slootweg et al” noted that irradiation failed to provide cure in ENHL of the oral cavity in more advanced clinical stages, whereas irradiation and resection provided permanent cure in all but 2 of 12 stage IE cases. McGurk et ali6 used local irradiation of tumor and local lymph nodes, whereas more extensive disease was treated with MOPP (mustine, vincristine, prednisolone, procarbicine) or COPad (cyclophosphamide, vincristine, prednisolone, adriamycin). An excellent review of reported rates of response and survival for patients with diffuse large-cell lymphoma treated with various chemotherapy regimens is summarized by Rusthoven.33 Eisenbud et al3 reported a 5-year disease-free rate of 40% (2/5 cases), and Robbins et al’ reported a 5-year disease-free rate of 50%, with 62% overall 5-year survival, in primary lymphoma of the mandible. In the current review of 23 patients with specified periods of survival, 9 died within 1 year of presentation of their disease. Slootweg et al” reported that clinical stage on presentation proved to be the major prognostic factor in ENHL of the oral tissues. A positive relationship between tumor response to initial treatment and overall prognosis in ENHL of the head and neck has also been shown. I6 Conflicting results exist with respect to prognosis for intraosseous tumors as compared with lymphomas in soft tissue sites. The number of mitotic tigures seen in biopsy samples of lymphomas of the oral cavity has shown good correlation to prognosis.‘* Summary A case involving primary lymphoma of the mandible is presented. The difficulties in diagnosis of this particular pathology are highlighted. The features of primary lymphoma of the mandible are described based on a review of the literature. Malignant lymphoma must be considered in the differential diagnosis of unexplained dental pain, swelling, ulceration, and radiographic evidence of rarefaction. References 1. Robbins KT, Fuller LM, Manning J, et al: Primary Ivmphoma of the mandible. Head Neck Surg 8: 192, 1988 2. Camubell RL. Kellev DE. Burkes EJ: Primarv reticulum cell sarcoma of the mandible. Oral Surg 39:919, 1975 3. Eisenbud L, Sciubba J, Mir R, et al: Oral presentations in non-Hodgkin’s lymphoma: A review of thirty-one cases. II. Fourteen cases arising in bone. Oral Surg Oral Med Oral Pathol 57:272. 1984
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4. Reiner DR, Chabner BA, Young RC, et al: Lymphomas presenting in bone: Results of histopathology staging and therapy. Ann Intern Med 87:50, 1977 5. Barker GR: Unifocal lymphomas of the oral cavity. Br J Oral Maxillofacial Surg 22:426, 1984 6. Eisenbud L, Sciubba J: Oral presentations in non-Hodgkin’s lymphoma: A review of thirty-one cases. I. Data analysis. Oral Sure Oral Med Oral Pathol 56: 151. 1983 7. Aozosa K, ?‘sujimoto M, Sukurai M, et al: Non-Hodgkin’s lymphoma in Osaka, Japan. Em J Cancer Clin Oncol 21:487, 1985 8. Freeman C, Berg JW, Cutler SJ: Occurrence and prognosis of extranodal lymphomas. Cancer 29:252. 1972 9. Takahashi H, Tezuka F, Fujita S, et al: Primary extranodal non-Hodgkin’s malignant lymphoma of the oral region: Analvsis of 11 autonsv cases. J Oral Path01 16:241, 1987 10. Slootweg PJ, Wittkampf AR, Kluin PM, et al: Extranodal non-Hodgkin’s lymphoma of the oral tissues. J Maxillofac Surg 13:85, 1985 1I. Tomich CE, Shafer WG: Lymphoproliferative disease of the hard palate. A clinicopathologic entity. Oral Surg 39:754, 1975 12. Fukuda Y, Ishida T, Fujimoto M, et al: Malignant lymphoma of the oral cavity: Clinicopathologic analysis of 20 cases. J Oral Pathol 16:8-12, 1987 13. Haidar Z: A review of non-Hodgkin’s lymphoma of the oral cavity 1950-1980. J Oral Med 41:197, 1986 14. Robbins KT, Fuller LM, Vlasak M, et al: Primary lymphomas of the nasal cavity and paranasal sinuses. Cancer 56:814, 1985 15. Kong JS, Fuller LM, Butler JJ, et al: Stages IE and HE non-Hodgkin’s lymphomas of Waldeyer’s ring and the neck. Am J Clin Oncol 7:629, 1984 16. McGurk M. Goepel JR, Hancock BW: Extranodal lymphoma of the head and neck: A review of 49 consecutive cases. Clin Radio1 36:455. 1985 17. Howell RE, Handlers JP, Abrams AM, et al: Extranodal oral lymphoma. II. Relationships between clinical features and the Lukes-Collins classification of 34 cases. Oral Surg Oral Med Oral Path01 64:597, 1987 18. Batsakis JG: Non-odontogenic tumors of the jaws, in Tu-
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19. 20. 21. 22.
23. 24. 25.
26.
27.
28.
29. 30.
31.
32.
33.
mars of the Head and Neck. Baltimore, MD, Williams & Wilkins, 1979, pp 381-419 Wang CC, Fleishil DJ: Primary reticulum cell sarcoma of bone. Cancer 28994, 1%8 Macintyre DR: Lymphomas of the mandible presenting as acute alveolar swellings. Br Dent J 161:25311986 Blake MN. Beck L: Reticulum cell sarcoma: Reoort of a case. J oral Surg 21:165, 1963 Sawyer R, Rosenthal DI, Maniglia AJ, et al: Unusual head and neck manifestations of non-Hodgkin’s lymphomas in children and adults. Laryngoscope 97: 1136, 1987 Slaughter DP, Economou SG, Smith HW: Surgical management of Hodgkin’s disease. Ann Surg 148:705, 1958 Larson DL, Robbins KT, Butler J: Lymphoma of the head and neck: A diagnostic dilemma. Am J Surg 148:433, 1984 Al-Soudani KA, Matukas VJ: Malignant lymphoma of the palate: Report of two cases. J Oral Maxillofac Surg 44:811, 1986 Carbone PP. Kaplan HS, Musshof K, et al: Report of the Committee on Hodgkin’s Disease Staging Classification. Cancer Res 31:1860, 1971 National Cancer Institute: Sponsored study of classifications of non-Hodgkin’s lymphomas: Summary and description of a working formulation for clinical usage. Cancer 49:2112, 1982 Rappaport H: Tumors of the Haematopoetic system. Washington, DC, Armed Forces Institute of Pathology, 1966, pp 91-206 Lukes RJ: The immunologic approach to the pathology of malignant lymphomas. Am J Clin Path01 72:657, 1979 Conley SF, Staszak C, Clamon GH et al: Non-Hodgkin’s lymphoma of the head and neck: The University of Iowa experience. Laryngoscope 97:291, 1987 Shirato H. Tsujii H, Arimoto T, et al: Early stage and neck non-Hodgkin’s lymphoma. The effect of tumor burden on prognosis. Cancer 58:2312, 1986 Lee YY, Van Tassel P, Nauert C, et al: Lymphomas of the head and neck: CT findings at initial presentation. AJR 149:575, 1987 Rusthoven JJ: Current approaches to the treatment of advanced stage non-Hodgkin’s lymphoma. Can Med Assoc J 136:29. 1987
Surg
1990
Microembolization and Resection of a Highly Vascular Pyogenic Granuloma DAVID FORMAN, DDS,* AND HERBERT I. GOLDBERG,
* In private practice, Langhome,
PA.
t Professor of Radiology and Neurosurgery,
Department of of Pennsylvania, Philadel-
Radiology, Hospital of theuniversity phia. Address correspondence and reprint requests to Dr Forman: Oxford Square, 360 Middletown Blvd, Suite 406, Langhome, PA 19047.
0
1990
American Association
geons 0278-2391/90/4804-0016$3.00/O
of Oral
and Maxillofacial
Sur-
MDt
Pyogenic granulomas are common oral lesions that usually present no unusual complications. The pathogenesis of this entity has not been fully understood, and multiple theories have been presented in the literature. The oral pyogenic granuloma is a benign soft tissue growth which can be sessile or pedunculated, and which bleeds readily with minor trauma. This lesion is also known as a pregnancy tumor since it often occurs in pregnant women, and
J Oral Maxillofac 48:409-415,
KATSIKERIS,
409
AND BROWN
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1990
Primary Lymphoma of the Mandible: Report of a Case A.W. GUSENBAUER,
DDS,* N.F. KATSIKERIS, DDS, DR DENT,t AND A. BROWN, DDS, FRCD(C)$
Primary lymphoma of the mandible is rare, and misdiagnosis is common.’ Definitive diagnosis can be diffkult to establish even when a biopsy specimen is representative of the lesion and preparation of the material is optimal.’ Predominant radiographic features include rarefaction representing tumor osteolysis or secondary osteomyelitis,2 but these are not specific to this particular pathology. Pain, mobility, and destructive lytic lesions associated with the teeth may mimic endodontic or periodontal pathosis, leading to incorrect diagnosis and inappropriate treatment.3 A case referred to our service for diagnosis and treatment of an apparent chronic infection of the mandible following multiple dental extractions is presented. The difficulties involved in the diagnosis and treatment of this case involving primary mandibular lymphoma and osteomyelitis are highlighted. A review of primary lymphoma of the mandible, based on cases reported in the literature, is also presented. Report of a Case A 53-year-old white man was referred to an oral surgeon by his dentist for treatment of an apparent chronic infection in the anterior mandible. The six mandibular anterior teeth had been extracted several months previously. A panoramic radiograph revealed an osteolytic lesion in the anterior part of the mandible. The patient was subsequently admitted to Toronto General Hospital for investigation and treatment, with the provisional diagnosis of osteomyelitis of the anterior mandible.
* Resident, Oral and Maxillofacial Surgery, University of Toronto, Toronto, Ontario, Canada. t Clinical Instructor, Department of Oral and Maxillofacial Surgery, University of Toronto Faculty of Dentistry, Toronto, Ontario, Canada. $ Staff Surgeon, Oral and Maxillofacial Surgery, Toronto General Hospital, Toronto, Ontario, Canada. Address correspondence and reprint requests to Dr Gusenbauer: 790 Mohawk Rd W, No. 909 Hamilton, Ontario, Canada L9C 6C6. 0 1990 geons
American
Association
0278-2391190/4804-0015$3.00/O
of Oral
and Maxillofacial
Sur-
Medical history revealed that the patient had been a heavy cigarette smoker for 35 years. The patient had suffered a mild myocardial infarction in 1985, and had a previous history of stomach ulcer and kidney stones. Physical examination on admission revealed an obese man with positive findings related to the orofacial region, but otherwise normal findings. Minor tenderness to palpation was noted in the mental region, and further examination revealed apparent expansion of the anterior mandible both buccally and inferiorly (Fig 1). No abnormalities of the overlying mucosa were noted. The lower six anterior teeth were absent. No palpable lymph nodes were detected. Routine laboratory examinations were all within normal limits, with the exception of an erythrocyte sedimentation rate (ESR) of 19 (male reference, O-10). Electrocardiogram (ECG) showed minor ST-T segment changes. On chest radiograph, the heart and mediastinum were normal, lungs and pleura were clear, and bones were involved. Some osteolytic bone destruction was evident in the chin area on a lateral cephalogram taken on admission (Fig 2). Computed tomography (CT) examination of the mandible showed an osteolytic area in the anterior part of the mandible with destruction of some areas of buccal cortical bone (Fig 3). The patient was taken to the operating room for surgical exploration and biopsy under general anesthesia. Subperiosteal dissection in the mandibular anterior region revealed connective tissue adherent to a thin buccal cortex of bone which was necrotic in appearance from the region of the left first premolar to the right first premolar. This region was decorticated, and the bone and overlying soft tissue were submitted for histologic examination. Specimens were taken for aerobic and anaerobic cultures. Further exploration showed that the inferior border of the mandible and lingual cortex were intact. The surgical site was irrigated and packed with BIPP iodoform gauze for daily change while the patient was in the hospital. The patient was discharged on the second postoperative day and reappointed for dressing change and follow-up in the outpatient clinic the following week. A diagnosis of chronic osteomyelitis was given on the preliminary pathology report. The final pathology report, following en toto examination of the remaining tissue, suggested the possibility that some atypical cells seen in clumps in the marrow spaces may be representative of a lymphoproliferative disorder. Further investigations to rule out malignant lymphoma were advised. The biopsy procedure of the involved bone in the anterior region of the mandible was repeated on an outpatient basis, and a diagnosis of immunoblastic or diffuse large cell lymphoma of the mandible was made. The pa-
410
PRIMARY LYMPHOMA OF THE MANDIBLE
FIGURE 1. Swelling of mandible in chin region. FIGURE 3. Destruction of buccal cortex of bone is evident on CT scan. tient was subsequently readmitted to the hospital for staging and treatment planning. Laboratory values were again within normal limits excepting an ESR of 19. The chest radiograph and ECG were unchanged. Examination on admission now revealed an area of surface erythema over rhe skin of the mental region and visible enlargement of the area. The patient described a dull, intermittent, poorly localized pain, nonradiating in nature, as well as bilateral mental nerve paresthesia. The patient had also noticed a bad taste in his mouth, although ulceration and sinus tracts were not apparent. Bone marrow aspiration and biopsy of the iliac spine revealed no evidence of involvement by malignant lymphoma. On CT, no evidence of metastatic disease was noted. Hematologic consultation and subsequent staging revealed that the patient’s disease was limited to the anterior part of the mandible.
The patient was presented at Lymphoma Conference, at which time a diagnosis of malignant primary nonHodgkin’s lymphoma of the mandible, stage IE, diffuse large-cell variety with aggressive histologic pattern, was made (Fig 4). The recent presence of chronic osteomyelitis led to a decision to begin treatment with chemotherapy alone, with possible radiotherapy at a later date, to decrease the possibility of osteoradionecrosis. The patient’s chemotherapy was initiated in the hospital, and consisted of a course of cyclophosphamide, adriamycin and vincristin, plus prednisolone. On l-week follow-up the jaw size was almost normal and the tissue was noticeably softer. The patient was continued on the chemotherapy regimen for 3 weeks, and subsequently received externalbeam radiation therapy. At 9-month follow-up there was no evidence of residual tumor, no lymphadenopathy, and no evidence of progression of disease to other sites. A CT taken at l-year follow-up showed signs of healing of the original lesion. The patient remains free of disease at 18
months postsurgery. Discussion
FIGURE 2. Lateral cephalogram shows osteolytic lesion in anterior part of the mandible.
The features of primary lymphoma of the mandible are summarized from a review of series presented in the literature (Table 1). Although primary osseous lymphoma may account for up to 15% of all extranodal lymphomas,4 the mandible is an infrequent presenting site. Barkes noted that the average time between presentation and definitive treatment of oral lymphoma was 2.5 months and felt that the similarity of presentation of oral lymphoma to other common dental diseases was in part responsible for this delay. Mobility of teeth, pain, and osteolytic lesions associated with the teeth and jaws may mimic periodontal or endodontic pathosis, thus leading to an erroneous diagnosis and inappropriate treatment .3 A delay of several months between presentation of the pa-
GUSENBAUER,
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AND BROWN
FIGURE 4. Histologic section showing large atypical cells and numerous mitotic ligures. (Hematoxylin-eosin stain. Original magnification, X240.)
tient to his dentist and referral to a specialist was noted in this case. Rarefaction in cases of malignant lymphoma of bone may represent tumor osteolysis or secondary Table 1.
osteomyelitis. The initial radiographic appearance of the present case was suggestive of osteomyelitis, and a similar appearance has been reported in severa1 such cases. On initial biopsy, osteomyelitis was
Primary Lymphoma of the Mandible: Reported Cases
Male/female Age (yr)
Campbell et al’
Eisenbud et al3
Eisenbud et al6
Robbins et al’
13/F 8-69
2/l 49
l/l 16
8/F 3-74
44
5
Macintyre”
l/l1 3/11 8111 l/l1 l/l1 IO/11
l/St l/St 4/5t
NS
19/21 12121 6121 6121 NS
213 l/3 l/3 l/3 l/3
212 l/2 212 l/2 l/2
Ill 1 6/ll 5/11 2111 NS
* Lesions may involve more than one anatomic location. t Results of 1984 and 1985 series combined.
Fukuda et al”
l/2 48
2/O 42
2/l 11
79
39
38
45
NS l/St 115t 4/5t
4116 3116 9/16 4116 4116 14/16
Slootweg et al”
l/l 52
29 Location* Ramus Angle Body Symphysis Anterior Posterior Stage I II III IV Clinical signs, symptoms Swelling Pain Numbness Loose teeth Lymphadenopathy
Howell et al”
Gusenbauer et al (this report) l/O 53
NS
212 l/l l/l 313 NS
212 l/2 o/2 o/2 012
313 l/3 l/3 NS NS
31/13 Avg 39.58 Median 42
51 NS
NS
Totals
1 1 0 0
NS NS NS NS NS
6132 II32 23134 II33 7142 35142 12124 4124 3124 5124
NS
NS NS NS NS
l/l O/l O/l 011 O/l
36143 22143 15143 1o/40 218
412
diagnosed and a suspicious clump of atypical cells was noted. The diagnosis, however, could not be made on initial biopsy. Robbins et al’ highlighted particular difficulty in diagnosis of primary lymphoma of the mandible. In a series of 11 patients, 5 patients could not be diagnosed on the basis of the initial biopsy. The investigators noted that all 5 patients requiring rebiopsy had lymphoma of the diffuse large-cell type. Our case required rebiopsy for definitive diagnosis and was also of the same histologic variety. The presence of concomitant osteomyelitis led to a modification of the usual combined therapy (chemotherapy and radiotherapy) in favor of chemotherapy alone in the initial phase of treatment to avoid possibility of osteoradionecrosis. Although extranoda! non-Hodgkin’s lymphoma (ENHL) of the head and neck area is common, the occurrence of malignant lymphoma of the oral cavity and pharynx is relatively rare.6 Aozosa et al7 found that oral malignant lymphoma (ML) represented 5% of a series of patients with ML of all varieties. In the series by Freeman et al* ML of the oral cavity comprised 2% of 1,467 patients with extranodal lymphoma. Takahashi et al9 reported that oral ENHL represented 8% of NHL and 37% of ENHL, whereas Barker’ stated that 20% to 34% of all ENHL occurs within the oral cavity when Waldeyer’s ring and the salivary glands are included. When considered in terms of total cases processed within oral pathology services, primary ENHL of the oral cavity represented only 0.2% and 0.1% of cases reported by Slootweg et al” and Tomich and Shafer, l1 respectively. The specific incidence of primary lymphoma arising in the mandible has not been addressed. Primary lymphoma of the mandible shows a 3 1: 13 male-female ratio, as summarized in Table 1. This is in agreement with Fukuda et al’s series of MLs of the oral cavity” (12:8 male-female ratio), although several other series of ML of the oral cavity report no significant sex predilection.10*‘3 Reported series of head and neck lymphomas have described both slight male predominance14*‘5 and slight female predominance. I6 The average age of presentation in the reviewed cases is 39.6 years, with a median age of 42 years. Peak incidence was in the 40- to 49-year age group, with 35% of cases occurring in the pre-30 age group and 35% in the post-50 age group. Series involving ML of the oral cavity have reported 60%” and 75%” of cases occurring in the over-50 age group. Howell et a1,l7 in reviewing the relationship between clinical features and the Lukes-Collins classification in 34 cases of extranodal oral lymphoma, found that patients with lymphoma composed of
PRIMARYLYMPHOMAOFTHEMANDIBLE
nontransformed follicular center cells had a greater mean age than those with tumors of transformed follicular cell centers or postfollicular cells. They also noted a trend of decreasing age of occurrence with increasing B cell transformation. The current review of primary lymphoma of the mandible did not contain sufficient cases classified according to the Lukes-Collins system to make this distinction. Mandibular lymphoma has been reported in the posterior part of the mandible in 37 cases, with only 7 cases involving the anterior portion of the mandible. Distribution by specific location within the mandible indicates that the body of the mandible is the most common location (23 cases), with the ramus angle and symphysis accounting for 6,7, and 8 cases, respectively. Numerous cases span these arbitrary anatomic divisions. Whereas the gastrointestinal (GI) tract is the major site of extranodal primary lymphomas,’ lymphoid aggregates which may undergo malignant transformation are also found in various head and neck locations. Within the oral cavity lymphoid aggregates are found in the floor of the mouth, lateral border and ventral surface of the tongue, buccal mucosa, tonsilar fauces, and hard and soft palate. Extranodal oral lymphoma may occur within soft tissue or bone. Fifteen per cent of Fukuda’s series occurred within bone,‘” as opposed to 35% in Howell’s series.17 Primary osseous lymphomas account for approximately 5% of all extranodal lymphomas.4 In the head and neck region, the maxilla is the most common site, and the mandible ranks second.” Within each of the LukesCollins classifications, the percentage of tumors that present with bony involvement appears to increase as the tumor category advances in B ceil transformation. l7 Swelling appears to be the most common presenting clinical finding in primary lymphoma of the mandible (84% of cases). Fukuda et alI2 also noted that a diffuse, painless swelling of the soft tissue was the initial presentation of most cases in his series of ML of the oral cavity. Pain was reported on initial clinical presentation in more than 50% of cases in the present review, whereas numbness (35%), loose teeth (25%), and cervical lymphadenopathy (12.5%) were less commonly reported clinical presentations. Hypoesthesia has been reported with or without radiographic evidence of involvement of the inferior alveolar canal. ’ Wang and Fleishil” noted that lymphoma occurring in osseous sites may extend into the medullary component or, in the case of the mandible, may involve the inferior alveolar canal, often without radiographic evidence of bony changes. The most common presentation of intraosseous lymphoma is rarefaction representing tumor osteolysis or sec-
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ondary osteomyelitis.2 Bony sclerosis at the periphery of the lesion has been reported in several reviews,’ whereas many cases present with a poorly defined diffuse margin without surrounding bone reaction.20 These features and a predilection for location in the premolar-molar region of the mandible are shared with intraosseous metastases.*’ Destruction of the lamina dura21 and pathologic fracture also have been described. Although resorption of tooth roots is not a common feature of intraosseous malignancies, isolated cases involving root resorption associated with lymphoma have been reported.‘*2’ Robbins et al’ noted one case involving the roots of a mandibular third molar in their series of primary lymphoma of the mandible. Other radiographic presentations noted in their series included diffuse osteolysis, focal osteolysis, widening of the mental foramen, and pathological fracture. In 2 of 11 cases there was no radiologic change. Slootweg et al” noted bony involvement in 16 of 20 cases of ENHL of the oral cavity, including several soft tissue cases exhibiting cortical erosion. They also noted that in 3 cases the initial radiographic appearance suggested periapical inflammation and had led to initial treatment consisting of extraction or periapical surgery. This appears to have been the presentation in our case as well. They also noted one mandibular lesion whose initial radiographic appearance had suggested osteomyelitis. A similar appearance was noted in the present case and osteomyelitis was, in fact, diagnosed on the original biopsy. Fukuda et al” noted destruction of neighboring bony structures in 4 of 11 malignant lymphomas of the gingiva. Table 2.
Definitive diagnosis of lymphoma may be difficult to establish even when optimal preparation of a representative specimen has been carried out.’ When nodal sites are involved, en toto excisional biopsy of involved nodes is preferred over incisional lymph node biopsy or needle biopsy in order to allow pathologic examination of the lymph node, capsule, and areas of normal and abnormal architecture side by side.22 Biopsy of the largest lymph node should be performed because surrounding nodes that may appear abnormal may simply show reactive hyperplasia.23 Extranodal lymphoma in the head and neck region may present a greater diagnostic challenge. This may be particularly evident when the disease is not suspected. 24 Interpretation of specimens from extranodal sites is also more difficult.’ Robbins et al’ discussed the necessity for removal of sufficient quantities of material in intraoral incisional biopsies to allow for histologic examination, including special stains, immunological studies for various surface markers, and electron microscopic investigation. Needle biopsy rarely provides sufficient material to fulfill these requirements. Areas to avoid on biopsy include previous biopsy sites with associated osteomyelitis, and other areas of inflammation. Superficial biopsies frequently identify only areas of chronic inflammation and necrosis.25 Based on the Ann Arbor Staging Classification,26 50% of cases of primary lymphoma of the mandible were classified as stage I (12/24 staged cases), 17% as stage II (4/24), 13% as stage III (3124)) and 21% as stage IV (5/24), on initial presentation. Considerable difficulty arises in summarizing the histopathologic findings of head and neck lymphomas due to
Histopathologic Classification of Reported Cases of Primary Lymphoma of the Mandible
Authot Eisenbud et al’
Rappaport Classification
NC1 Working Formulation
Lukes-Collins Classification
Diffuse histiocytic Diffuse, poorly differentiated lymphocytic Burkitt’s
2 2
Diffuse large cell Diffuse small cleaved
2 2
I
1
Eisenbud et al6
Diffuse lymphoblastic Burkitt’s
1 1
Slootweg et al’”
Diffuse mixed
1
Small noncleaved Burkitt’s Diffuse lymphoblastic Small noncleaved Burkitt’s Diffuse mixed small and large Diffuse large cell
Robbins et al’
Diffuse histiocytic Diffuse large cell Diffuse undifferentiated Burkitt’s Unclassified
1
1 1 1 1
7 2
1 I Diffuse small noncleaved Diffuse large noncleaved
Howell et al” Gusenbauer et al (this report)
Diffuse large cell
1
2
1
414 the number of different classification schemes used. Table 2 summarizes the histopathologic findings of reported cases of primary lymphoma of the mandible according to the NC1 Working Formulation,27 Rappaport Classification,28 or Lukes-Collins system.29 Within the NC1 classification, lymphoma of the diffuse large-cell type predominates. This appears to be consistent with series involving head and neck lymphomas,30-32 series involving the oral cavity in general,‘0,‘2 and also reflects the findings of Slootweg et al, lo who found that 8 of 14 cases of ENHL of the oral cavity arising specifically within bone were of the diffuse large-cell variety. By Rappaport classification, 3 of 9 cases arising within the mandible were classified as diffuse histiocytic. It appears that the relative predominance of this type is not confined to the mandible, the oral cavity, or the head and neck, but appears to be a feature of non-Hodgkin’s lymphoma (NHL) in general. lo Numerous series have shown a significant incidence of abdominal lesions as a first manifestation of progressive disease in patients with head and neck lymphoma. 3’ Takahashi et a1,9 based on autopsy findings, concluded that primary oral lymphoma spread via three modes: 1) lymphatic spread via cervical lymph nodes and intrathoracic and abdominal nodes to extranodal organs, 2) contiguous spread to adjacent organs, and 3) blood-borne distant metastases in late disease. The lung, kidneys, pancreas, liver, spleen, heart, GI tract, bone marrow, and adrenal glands were the most commonly involved viscera. This pattern of dissemination of primary ENHL of the oral cavity appears to behave like oral carcinoma with metastatic spread along primary drainage areas.31 Robbins et al’ noted spread of primary lymphoma of the mandible to cervical lymph nodes in 3 of 11 cases, pulmonary parenchyma in 1 of 11 cases, and liver in 1 of 11 cases. Although cervical lymphadenopathy was reported clinically in 12.5% of the cases presently reviewed, it is uncertain what proportion comprised reactive lymphadenopathy and what proportion represented true progression of disease. Various treatment regimens for head and neck lymphomas have been used and usually consist of irradiation, radiotherapy, surgery, or combinations of these. Most patients with NHL limited to the head and neck can be treated with radiotherapy with good results. Although chemotherapy is indicated in disseminated cases, recent trends at many centers is toward combined therapy for such cases, whereas surgery is generally reserved for excisable lesions.7 Conley et a130stated that combined therapy has been shown to offer the best prognosis in patients with intermediate- to high-grade histologic
PRIMARY LYMPHOMA OF THE MANDIBLE
types in a review of series of several investigators. Localized stage I and IE cases were treated with radiotherapy primarily, whereas patients with stage II to IV were treated with CHOP (cyclophosphamide, hydroxyldaunorubicin [doxorubicin], vincristine [oncovin], and prednisone) chemotherapy and irradiation. Slootweg et al” noted that irradiation failed to provide cure in ENHL of the oral cavity in more advanced clinical stages, whereas irradiation and resection provided permanent cure in all but 2 of 12 stage IE cases. McGurk et ali6 used local irradiation of tumor and local lymph nodes, whereas more extensive disease was treated with MOPP (mustine, vincristine, prednisolone, procarbicine) or COPad (cyclophosphamide, vincristine, prednisolone, adriamycin). An excellent review of reported rates of response and survival for patients with diffuse large-cell lymphoma treated with various chemotherapy regimens is summarized by Rusthoven.33 Eisenbud et al3 reported a 5-year disease-free rate of 40% (2/5 cases), and Robbins et al’ reported a 5-year disease-free rate of 50%, with 62% overall 5-year survival, in primary lymphoma of the mandible. In the current review of 23 patients with specified periods of survival, 9 died within 1 year of presentation of their disease. Slootweg et al” reported that clinical stage on presentation proved to be the major prognostic factor in ENHL of the oral tissues. A positive relationship between tumor response to initial treatment and overall prognosis in ENHL of the head and neck has also been shown. I6 Conflicting results exist with respect to prognosis for intraosseous tumors as compared with lymphomas in soft tissue sites. The number of mitotic tigures seen in biopsy samples of lymphomas of the oral cavity has shown good correlation to prognosis.‘* Summary A case involving primary lymphoma of the mandible is presented. The difficulties in diagnosis of this particular pathology are highlighted. The features of primary lymphoma of the mandible are described based on a review of the literature. Malignant lymphoma must be considered in the differential diagnosis of unexplained dental pain, swelling, ulceration, and radiographic evidence of rarefaction. References 1. Robbins KT, Fuller LM, Manning J, et al: Primary Ivmphoma of the mandible. Head Neck Surg 8: 192, 1988 2. Camubell RL. Kellev DE. Burkes EJ: Primarv reticulum cell sarcoma of the mandible. Oral Surg 39:919, 1975 3. Eisenbud L, Sciubba J, Mir R, et al: Oral presentations in non-Hodgkin’s lymphoma: A review of thirty-one cases. II. Fourteen cases arising in bone. Oral Surg Oral Med Oral Pathol 57:272. 1984
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4. Reiner DR, Chabner BA, Young RC, et al: Lymphomas presenting in bone: Results of histopathology staging and therapy. Ann Intern Med 87:50, 1977 5. Barker GR: Unifocal lymphomas of the oral cavity. Br J Oral Maxillofacial Surg 22:426, 1984 6. Eisenbud L, Sciubba J: Oral presentations in non-Hodgkin’s lymphoma: A review of thirty-one cases. I. Data analysis. Oral Sure Oral Med Oral Pathol 56: 151. 1983 7. Aozosa K, ?‘sujimoto M, Sukurai M, et al: Non-Hodgkin’s lymphoma in Osaka, Japan. Em J Cancer Clin Oncol 21:487, 1985 8. Freeman C, Berg JW, Cutler SJ: Occurrence and prognosis of extranodal lymphomas. Cancer 29:252. 1972 9. Takahashi H, Tezuka F, Fujita S, et al: Primary extranodal non-Hodgkin’s malignant lymphoma of the oral region: Analvsis of 11 autonsv cases. J Oral Path01 16:241, 1987 10. Slootweg PJ, Wittkampf AR, Kluin PM, et al: Extranodal non-Hodgkin’s lymphoma of the oral tissues. J Maxillofac Surg 13:85, 1985 1I. Tomich CE, Shafer WG: Lymphoproliferative disease of the hard palate. A clinicopathologic entity. Oral Surg 39:754, 1975 12. Fukuda Y, Ishida T, Fujimoto M, et al: Malignant lymphoma of the oral cavity: Clinicopathologic analysis of 20 cases. J Oral Pathol 16:8-12, 1987 13. Haidar Z: A review of non-Hodgkin’s lymphoma of the oral cavity 1950-1980. J Oral Med 41:197, 1986 14. Robbins KT, Fuller LM, Vlasak M, et al: Primary lymphomas of the nasal cavity and paranasal sinuses. Cancer 56:814, 1985 15. Kong JS, Fuller LM, Butler JJ, et al: Stages IE and HE non-Hodgkin’s lymphomas of Waldeyer’s ring and the neck. Am J Clin Oncol 7:629, 1984 16. McGurk M. Goepel JR, Hancock BW: Extranodal lymphoma of the head and neck: A review of 49 consecutive cases. Clin Radio1 36:455. 1985 17. Howell RE, Handlers JP, Abrams AM, et al: Extranodal oral lymphoma. II. Relationships between clinical features and the Lukes-Collins classification of 34 cases. Oral Surg Oral Med Oral Path01 64:597, 1987 18. Batsakis JG: Non-odontogenic tumors of the jaws, in Tu-
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19. 20. 21. 22.
23. 24. 25.
26.
27.
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29. 30.
31.
32.
33.
mars of the Head and Neck. Baltimore, MD, Williams & Wilkins, 1979, pp 381-419 Wang CC, Fleishil DJ: Primary reticulum cell sarcoma of bone. Cancer 28994, 1%8 Macintyre DR: Lymphomas of the mandible presenting as acute alveolar swellings. Br Dent J 161:25311986 Blake MN. Beck L: Reticulum cell sarcoma: Reoort of a case. J oral Surg 21:165, 1963 Sawyer R, Rosenthal DI, Maniglia AJ, et al: Unusual head and neck manifestations of non-Hodgkin’s lymphomas in children and adults. Laryngoscope 97: 1136, 1987 Slaughter DP, Economou SG, Smith HW: Surgical management of Hodgkin’s disease. Ann Surg 148:705, 1958 Larson DL, Robbins KT, Butler J: Lymphoma of the head and neck: A diagnostic dilemma. Am J Surg 148:433, 1984 Al-Soudani KA, Matukas VJ: Malignant lymphoma of the palate: Report of two cases. J Oral Maxillofac Surg 44:811, 1986 Carbone PP. Kaplan HS, Musshof K, et al: Report of the Committee on Hodgkin’s Disease Staging Classification. Cancer Res 31:1860, 1971 National Cancer Institute: Sponsored study of classifications of non-Hodgkin’s lymphomas: Summary and description of a working formulation for clinical usage. Cancer 49:2112, 1982 Rappaport H: Tumors of the Haematopoetic system. Washington, DC, Armed Forces Institute of Pathology, 1966, pp 91-206 Lukes RJ: The immunologic approach to the pathology of malignant lymphomas. Am J Clin Path01 72:657, 1979 Conley SF, Staszak C, Clamon GH et al: Non-Hodgkin’s lymphoma of the head and neck: The University of Iowa experience. Laryngoscope 97:291, 1987 Shirato H. Tsujii H, Arimoto T, et al: Early stage and neck non-Hodgkin’s lymphoma. The effect of tumor burden on prognosis. Cancer 58:2312, 1986 Lee YY, Van Tassel P, Nauert C, et al: Lymphomas of the head and neck: CT findings at initial presentation. AJR 149:575, 1987 Rusthoven JJ: Current approaches to the treatment of advanced stage non-Hodgkin’s lymphoma. Can Med Assoc J 136:29. 1987
Surg
1990
Microembolization and Resection of a Highly Vascular Pyogenic Granuloma DAVID FORMAN, DDS,* AND HERBERT I. GOLDBERG,
* In private practice, Langhome,
PA.
t Professor of Radiology and Neurosurgery,
Department of of Pennsylvania, Philadel-
Radiology, Hospital of theuniversity phia. Address correspondence and reprint requests to Dr Forman: Oxford Square, 360 Middletown Blvd, Suite 406, Langhome, PA 19047.
0
1990
American Association
geons 0278-2391/90/4804-0016$3.00/O
of Oral
and Maxillofacial
Sur-
MDt
Pyogenic granulomas are common oral lesions that usually present no unusual complications. The pathogenesis of this entity has not been fully understood, and multiple theories have been presented in the literature. The oral pyogenic granuloma is a benign soft tissue growth which can be sessile or pedunculated, and which bleeds readily with minor trauma. This lesion is also known as a pregnancy tumor since it often occurs in pregnant women, and
