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Ovarian Non-Hodgkin’s Lymphoma: A Clinicopathologic Study of Eight

Primary Cases

Article  in  Modern Pathology · December 2001

DOI: 10.1038/modpathol.3880442 · Source: PubMed

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Ovarian Non-Hodgkin’s Lymphoma: A ClinicopathologicStudy of Eight Primary CasesRussell Vang, M.D., L. Jeffrey Medeiros, M.D., Roger A. Warnke, M.D., John P. Higgins, M.D.,Michael T. Deavers, M.D.

Stanford University Medical Center (RV, RAW, JPH), Department of Pathology (Laboratory of SurgicalPathology), Stanford, California; and The University of Texas-M.D. Anderson Cancer Center (JM, MTD),Houston, Texas

Primary (localized) non-Hodgkin’s lymphoma(NHL) of the ovary is rare. We studied eight cases ofprimary ovarian NHL to better understand the clin-icopathologic and immunophenotypic features ofthese tumors. The patients ranged in age from 29 to62 years (mean 47 years). Pelvic complaints werethe most common symptoms; however, three ofeight neoplasms were discovered incidentally. Alltumors were unilateral and Ann Arbor stage IE. Thethree incidental NHL were microscopic (largest 1.2cm), whereas the grossly evident lesions rangedfrom 7.5 to 20 cm (mean 13.3). Each tumor wasclassified according to the World Health Organiza-tion Classification as follows: diffuse large B-celllymphoma (three cases), follicular lymphoma (twocases), Burkitt lymphoma (one case), T-cell anaplas-tic large cell lymphoma (one case), and precursorT-lymphoblastic lymphoma (one case). Six tumorswere of B-cell lineage, and two tumors were of T-celllineage. All three diffuse large B-cell lymphomaswere positive for BCL-6, two were positive for CD10,and two were positive for BCL-2. Estrogen and pro-gesterone receptors were negative in all NHLs as-sessed. Patients were treated by various combina-tions of surgery, chemotherapy, and radiotherapy.Clinical follow-up ranged from 1.3 to 11.7 years(mean 5.2) and all patients were alive without dis-ease at last follow-up. We conclude that most pa-tients with primary ovarian NHL present withsymptoms attributable to an ovarian mass, but in asubset of patients ovarian NHL may be detectedincidentally. With appropriate therapy, patients ap-pear to have a favorable prognosis althoughfollow-up is short for some patients in this study.

KEY WORDS: Gynecologic, Immunohistochemistry,Lymphoma, Ovary.

Mod Pathol 2001;14(11):1093–1099

Non-Hodgkin’s lymphoma (NHL) may involve thegynecologic tract, and the ovary is one of the morecommon anatomic sites to be involved. Ovarianinvolvement by NHL is usually secondary, occur-ring as a part of systemic disease. Localized, pre-sumably primary, NHL of the ovary is rare (1).

Previous reports of ovarian NHL have includedboth primary and secondary cases. In these studies,primary NHLs of the ovary represent only a minor-ity of the cases reported, usually less than 10%.Thus, secondary cases have been well characterizedin the literature (2, 3), but information about pri-mary cases is limited.

Furthermore, several reported cases of primaryovarian NHL did not have adequate Ann Arbor stag-ing information, and therefore may not have beentruly localized. For these reasons, we chose to col-lect well-characterized cases of primary ovarianNHL to describe their clinicopathologic and immu-nophenotypic features.

MATERIALS AND METHODS

Cases of primary NHL of the ovary were identi-fied from the surgical pathology files of StanfordUniversity Medical Center and The University ofTexas-M.D. Anderson Cancer Center. These casesincluded both in-house surgical specimens andconsultation cases. We collected low-stage cases,designated as Ann Arbor stage IE after clinicopath-ologic staging, and considered these tumors to beprimary. In contrast, we considered NHL involvingthe ovary as a part of Ann Arbor stage IIIE and IVdisease to probably represent secondary involve-ment and excluded those cases from the study.However, we acknowledge that by using these def-initions, any NHL that arose in the ovary and sub-sequently disseminated would be eliminated from

Copyright © 2001 by The United States and Canadian Academy ofPathology, Inc.VOL. 14, NO. 11, P. 1093, 2001 Printed in the U.S.A.Date of acceptance: July 21, 2001.Address reprint requests to: Michael T. Deavers, M.D., The University ofTexas-M.D. Anderson Cancer Center, Department of Pathology, Box 85,1515 Holcombe Boulevard, Houston, TX 77030-4095; e-mail:mdeavers@notes.mdacc.tmc.edu.

1093

our study. We did not encounter any stage IIE cases.Four cases were previously reported in a clinico-pathologic review of NHL involving the gynecologictract (1), and the clinical features of three of thesecases were also reported elsewhere (4).

Clinical information was obtained by review ofthe medical chart and correspondence with the cli-nician. Histologic features were studied using sec-tions routinely stained with hematoxylin-eosin.Each neoplasm was classified according to the re-cently proposed World Health Organization Classi-fication (5).

Immunohistochemical studies were performedusing formalin-fixed, paraffin-embedded tissuesections and a variable panel of antibodies specificfor the following antigens: CD3, CD20, CD21, CD30,CD99, BCL-2, BCL-6, and ALK-1 (DAKO, Carpinte-ria, CA); CD10 (Novocastra, Burlingame, CA); CD43(Becton Dickinson, Franklin Lakes, NJ); estrogenand progesterone receptors (Ventana, Tucson, AZ);and TdT (SuperTechs, Bethesda, MD).

RESULTS

Clinical FeaturesEight cases of localized ovarian NHL, all Ann

Arbor stage IE, were included in this study. Thepatients ranged in age from 29 to 62 years (mean 47years). The most common presenting signs orsymptoms were: pelvic pain (n � 2); pelvic mass (n� 1); and urinary frequency and incontinence (n �1). One patient presented with constitutional symp-toms that were not otherwise specified. Three pa-

tients had neoplasms that were detected as inci-dental findings. Two of these patients underwenttotal abdominal hysterectomy and bilateralsalpingo-oophorectomy for uterine leiomyomas,and one patient had excision of an endometrioticcyst within which NHL was identified in the cystwall. All of the neoplasms were unilateral; sevenwere right-sided and one involved the left ovary.The three incidental tumors were microscopic(�1.2 cm), and no lesion was observed grossly. Fiveneoplasms were grossly identified and ranged insize from 7.5 to 20 cm (mean 13.3).

Treatment consisted of various combinations ofsurgery, chemotherapy, and radiotherapy. Sevenpatients were treated surgically: five underwent to-tal abdominal hysterectomy and bilateral salpingo-oophorectomy, and two underwent bilateralsalpingo-oophorectomy. Seven and two patients,respectively, received chemotherapy and radiother-apy. Clinical follow-up ranged from 1.3 to 11.7 years(mean 5.2 years). All patients were alive, relapse-free, and disease-free at last follow-up.

Histologic and Immunohistochemical Findings(Table 1)

[Table 1] Three tumors (Cases 3, 4, and 7) werediffuse large B-cell lymphoma (DLBCL). Two DL-BCL had entirely diffuse architecture, while approx-imately 25 to 50% of one DLBCL (Case 7) containedfollicular areas. All of the DLBCL consisted of sheetsof large lymphoid cells with a moderate amount ofpale cytoplasm. The nuclei were round or had ir-

TABLE 1. Primary (Stage IE)Non-Hodgkin’s Lymphoma of the Ovary

CaseNo.

Age(y)

Presentation Side Size (cm) DiagnosisImmunophenotype

Therapy Follow-UpLineage CD10 CD99 Bcl-2 Bcl-6

1 29 Pelvic pain R 13 T-LBL T-cell � � ND � TAH-BSO,CT

NED, 5.8 y

2 39 Incidentalfinding

R Microscopic ALCL T-cell ND ND ND ND TAH-BSO NED, 4 y

3 41 Urinaryfrequency,incontinence

L 18 DLBCL B-cell � � � � BSO, CT,RT

NED, 5.5 y

4 43 Pelvic pain R 8 DLBCL B-cell � � � � TAH-BSO,CT

NED, 6 y

5 50 Incidentalfinding

R Microscopic Follicularlymphoma,Grade 2

B-cell � � � � TAH-BSO,CT

NED, 3.5 y

6 51 Incidentalfinding

R Microscopic Follicularlymphoma,Grade 3

B-cell � � � � TAH-BSO,CT

NED, 1.3 y

7 59 Pelvic mass R 7.5 DLBCLwithfollicularareas

B-cell � � � � BSO, CT NED, 3.5 y

8 62 Constitutionalsymptoms,NOS

R 20 BurkittLymphoma

B-cell � � ND � CT, RT NED, 11.7 y

ALCL, anaplastic large cell lymphoma; BSO, bilateral salpingo-oophorectomy; CT, chemotherapy; DLBCL, diffuse large B-cell lymphoma; ER, estrogenreceptor; ND, not done; NED, no evidence of disease; NOS, not otherwise specified (detailed clinical information of presentation not available); PR,progesterone receptor; RT, radiotherapy; TAH, total abdominal hysterectomy; T-LBL, precursor T-lymphoblastic lymphoma; �, positive; �, negative.

1094 Modern Pathology

regular nuclear contours, irregularly distributedchromatin, nucleoli, and many mitoses (Fig. 1). Thefollicular areas in Case 7 were composed of cellssimilar to those seen in the diffuse areas of thetumor. Areas of necrosis and sclerosis were ob-served. All three DLBCL were positive for CD20 andBCL-6, two cases were positive for CD10, and twocases were positive for BCL-2. The DLBCL withfollicular areas was negative for BCL-2.

Two cases (Cases 5 and 6) were follicular lympho-mas. Case 5 was Grade 2, with a mixture of smallcleaved and atypical large cells. Case 6 was Grade 3(Fig. 2), with a predominance of large cleaved cells.Both cases were positive for CD10, CD20, andBCL-6 and negative for BCL-2. Staining for CD21 inCase 6 highlighted a network of follicular dendriticcells in follicles; the neoplastic cells were negative.

One case each was classified as Burkitt lym-phoma, T-cell anaplastic large cell lymphoma(ALCL), and T-precursor lymphoblastic lymphoma(T-LBL). The Burkitt lymphoma showed a starry-skybackground and was composed of a relatively mo-notonous population of intermediately-sized neo-plastic cells. These cells had round to slightly irreg-ular nuclear contours, an extremely high mitoticrate, and some cells had vesicular chromatin (Fig. 3,A–B). Thus, this tumor fits within the category ofatypical Burkitt lymphoma (previously designatedas Burkitt-like) in the WHO classification (4). Thistumor was positive for CD20 and BCL-6 but failedto stain for CD10. The T-cell ALCL was composed ofsheets of large round cells with a moderate amountof amphophilic cytoplasm. The nuclei were large,ovoid, and vesicular with large nucleoli. This neo-plasm was positive for CD43 and CD30, but wasnegative for ALK-1. The T-LBL was diffuse and com-posed of small cells with minimal cytoplasm thatinfiltrated collagen in a single file (“indian file”)pattern. The nuclei were round and convoluted.

The chromatin was fine with inconspicuous nucle-oli and mitoses were numerous (Fig. 4). The neo-plastic cells were positive for CD3, CD10, CD99, andTdT and were negative for BCL-6.

CD99 was assessed in seven tumors, one T-LBL(discussed above) and six B-cell NHL tumors: threeDLBCL, two follicular lymphomas, and one Burkittlymphoma (Cases 3 to 8). All six B-cell neoplasmswere negative for CD99. Residual ovarian stroma inthe hilum and reactive small lymphocytes withinthe lymphomatous infiltrate, were CD99-positive.Stains for estrogen (eight cases tested) and proges-terone (seven cases tested) receptors were negativein all cases assessed.

DISCUSSION

NHL uncommonly involves the gynecologic tract.However, when involved by NHL, the ovary is oneof the more common anatomic sites. Previous stud-ies of NHL involving gynecologic sites (1–3) haveshown that most NHL involving the ovary are sys-temic tumors, of which ovarian involvement is onlyone aspect. Less than 10% of all ovarian NHLs re-ported have been localized, presumably arising inthe ovary.

In the current study, we collected eight localized(Ann Arbor stage IE) ovarian NHL, which appear tohave arisen in the ovary, to further understand theirclinicopathologic and immunophenotypic features.The mean age of the patients was 47 years. Patientsusually sought medical attention for pelvic com-plaints, but in three patients the NHL was discov-ered as an incidental finding during the work-up ofother gynecologic diseases. The incidental neo-plasms were microscopic, whereas the grossly iden-tified lesions were large, up to 20 cm. The mostcommon types were DLBCL (three cases) and fol-licular lymphoma (two cases), and six of eight NHLwere of B-cell lineage. The patients were treated invarious fashions and all were disease free with amean follow-up of 5.2 years.

There is a suggestion in the literature that hor-mone receptors may be expressed by some hema-topoietic neoplasms. Although two primary ovarianNHL studied by Monterroso et al. (2) failed to ex-press estrogen receptors, others have shown estro-gen and progesterone receptor expression in pa-tient samples and cell lines of plasma cell myeloma,T-cell leukemia/lymphoma, acute myeloid leuke-mia, and B-cell chronic lymphocytic leukemia, asdetermined by immunocytochemical and bio-chemical assays (6 –9). Because the NHL in ourseries presumably arose within the gynecologictract, we assessed for the presence of estrogen andprogesterone receptors. All cases were negative.Thus, there is no immunohistochemical support ofFIGURE 1. Diffuse large B-cell lymphoma (Case 4).

Primary Ovarian Lymphoma (R. Vang et al.) 1095

a role for estrogen or progesterone in the pathogen-esis of primary NHL of the ovary.

The histogenesis of primary ovarian NHL is per-plexing. In normal ovaries, lymphocytes of B-celland T-cell lineage are present within “cortical gran-ulomas,” and rare lymphocytes are dispersed

throughout the ovarian stroma and within ovarianfollicles and corpora lutea (10). We considered thepossibility that chronic inflammation involving theovaries predisposes to the development of NHL,analogous to low-grade B-cell MALT-lymphoma in-volving the stomach (11). However, in seven cases

FIGURE 2. Follicular lymphoma, Grade 3. A, Follicular architecture. B, Cytologic features (Case 6).

FIGURE 3. Burkitt lymphoma. A, Starry sky pattern. B, Cytologic features (Case 8).

1096 Modern Pathology

there was no clinical or histologic evidence of in-flammation. In the ALCL, a background of dis-persed plasma cells and eosinophils of mild densitywas present within the wall of the endometrioticcyst. Thus, there is no obvious role for chronicinflammation in the pathogenesis of these tumors.

One of the findings in this series is that manycases of localized ovarian NHL are of follicle centerorigin. Three of eight (38%) NHLs in this study hadobvious follicular differentiation: two cases of fol-licular lymphoma (Cases 5 and 6) and one DLBCLwith follicular areas (Case 7). Also, the results of thestaining for CD10 and BCL-6 in our series maysuggest follicle center derivation for primary ovar-ian DLBCL. All three tumors expressed CD10and/or BCL-6. CD10 expression in non-neoplasticlymph nodes is confined predominantly to germi-nal centers and CD10 is also commonly expressedin follicular lymphomas (12, 13). Likewise, expres-sion of BCL-6, positive in all three DLBCL in thisstudy, is restricted to centroblasts and centrocytesof germinal centers (14), and is commonly ex-pressed by follicular lymphomas and DLBCL of fol-licle center origin (14, 15). Thus, the presence ofCD10 and/or BCL-6 expression in the DLBCL of thisstudy supports follicle center origin, as suggestedby others (12–15). The relatively high frequency ofovarian NHL of possible follicle center origin foundin this study has not been previously noted in theliterature (Table 2). The explanation for this is un-certain, but in most prior studies antibodies spe-cific for CD10 and BCL-6 that could be applied tofixed, paraffin-embedded tissue sections were notavailable.

Although 85% of nodal follicular lymphomasoverexpress BCL-2 (16) as a result of t(14;18), follic-ular lymphomas arising in extranodal sites are lessoften BCL-2-positive. Thus absence of BCL-2 ex-pression, as in the follicular areas of Cases 5 to 7 in

this study, may be a feature of primary follicularlymphoma of the ovary, analogous to follicular lym-phomas arising in other extranodal sites (17). How-ever, the follicular areas in our cases containedincreased numbers of large cells, and it is knownthat BCL-2 is expressed less often in Grade 3 follic-ular lymphoma (16, 17). Alternatively, our findingscould suggest that the bcl-2 gene does not play arole in the pathogenesis of primary ovarian follicu-lar lymphoma. Further molecular investigation toaddress this possibility has not been done.

A summary of 19 cases of primary ovarian NHL(Ann Arbor stages IE or IIE) NHL (2, 18 –29) from theliterature is listed in Table 2. Some cases originallypublished using FIGO staging, but for which there isinsufficient information to translate into the AnnArbor system have not been included (3). The find-ings in our study are somewhat comparable. Thepatients have a wide age range, and most patientspresent with pelvic or abdominal complaints. How-ever, it is noteworthy that almost one third of casesare detected as incidental findings. The incidentalneoplasms may arise in unusual settings, such aswithin the wall of an ovarian endometriotic cyst(Case 2 of this study), or associated with a maturecystic teratoma (20) or serous borderline tumor(26). Bilaterality is infrequent, and neoplasms maybe microscopic or extremely large. DLBCL appearsto be the most common type of primary ovarianNHL. This is also true for other primary NHL arisingin other sites within the female genital tract (30 –32). Slight differences between the survival of pa-tients in our series, 100% at 5 years, and that ofpatients reported in the literature, 80% at 5 years,may be due to a paucity of cases with follow-uplonger than 5 years. Only one patient with primaryovarian NHL has died. However, the follow-up isrelatively short for several cases in our series, aswell as for those from the literature. Longerfollow-up is needed to more reliably determine thelong-term behavior of these lesions.

Histologically similar neoplasms that should bedifferentiated from NHL involving the ovary in-clude adult granulosa cell tumor, dysgerminoma,small cell carcinoma of hypercalcemic type (33),and granulocytic sarcoma. Depending on the indi-vidual case, other less histologically problematiclesions that may be included in the differential di-agnosis are poorly differentiated surface-epithelialor metastatic carcinomas, undifferentiated carci-noma (34), small cell carcinoma of pulmonary type(35), inflammatory pseudotumor, primitive neuro-ectodermal tumor (PNET), other non-PNET neuro-ectodermal tumors (36), variants of malignant me-sodermal mixed tumor with scarce epithelialelements and numerous round cells, endometrioidstromal sarcoma, rhabdomyosarcoma, intra-abdominal desmoplastic small round cell tumor,

FIGURE 4. Precursor T-lymphoblastic lymphoma (Case 1).

Primary Ovarian Lymphoma (R. Vang et al.) 1097

poorly-differentiated Sertoli-Leydig cell tumor (37),and melanoma. These may be distinguished fromprimary ovarian NHL by considering the clinicalinformation, histologic features, and immunohisto-chemical profiles.

In summary, primary ovarian NHL is rare. Pa-tients usually present because of pelvic complaints,but some cases may be detected as an incidentalfinding. The neoplasms may be microscopic or verylarge and are usually unilateral. Both B-cell andT-cell NHL can arise in the ovary, but B-cell tumorsare most common, and many appear to be of folli-cle center origin. Patients with primary ovarianNHL appear to have a good prognosis, although theclinical follow-up in our study is relatively short.

Acknowledgments: The authors thank the followingphysicians for their contribution of material and/orinformation for this study: Alosio Graca Aranha (Riode Janeiro, Brazil), Ierece Aymore (Rio de Janeiro,Brazil), James Breeden (Carson City, NV), PhillipDeos (Modesto, CA), Heber E. Dunaway (Metairie,LA), Larry Erickson (Modesto, CA), Jeffrey Goates(Denver, CO), Hal Levy (Denver, CO), and JohnSiebel (Palo Alto, CA).

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1098 Modern Pathology

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