Marginal Zone B-Cell Lymphoma With Monocytoid B ...

HEMATOPATHOLOGY Original Article

Marginal Zone B-Cell Lymphoma With Monocytoid B-Cell Lymphocytes in Pediatric Patients Without Immunodeficiency A Report of Two Cases KOJO S. J. ELENITOBA-JOHNSON, MD, SHIMAREET KUMAR, MD, MEGAN S. LIM, MD, DOUGLAS W. KINGMA, MD, MARK RAFFELD, MD, AND ELAINE S. JAFFE, MD spreads revealed trisomy 13 (karyotype 47, XY,+13). Although trisomy 13 has been described in association with acute nonlymphocytic leukemias and myelodysplastic syndromes, this case represents the first documented association of trisomy 13 with marginal zone B-cell lymphoma. Interphase cytogenetics analysis for trisomy 3, reported to be associated with mucosa-associated lymphoid tissue (MALT) lymphomas, was negative in both cases. Although low-grade lymphomas of the MALT type have been reported in HIV-positive patients, the two cases reported here are unique in that they occurred in young patients without HIV infection or any other evidence of immunodeficiency. (Key words: Malignant lymphoma; Marginal zone B-cell lymphoma; Monocytoid B-cells) Am J Clin Pathol 1997;107:92-98.

In 1986, Sheibani et al 1 reported a series of morphologically distinct low-grade B-cell neoplasms that they referred to as monocytoid B-cell l y m p h o m a (MBCL). These tumors are thought to be neoplastic expansions derived from monocytoid B lymphocytes (MBLs), which typically exhibit a homing tendency to the parafollicular B-cell zone, marginal zone, and subcapsular sinuses. 2 Early descriptions of these cells in the lymph node sinuses and their resemblance to h i s t i o c y t e s s u g g e s t e d a histiocytic d e r i v a t i o n . However, because they lacked both phagocytic activity and lysozomal e n z y m e s such as nonspecific esterase and acid phosphatase, Lennert 3 initially pro-

posed they might be immature sinus histiocytes. Subsequently, the demonstration of expression of pan-B-cell antigens and immunoglobulin light chains and negative immunoreactivity with T-cell and histiocytic markers, have indicated a B-cell lineage. MBLs also have been referred to as parafollicular B cells, reflecting their microanatomic predilection for the parafollicular zone of the lymph node. 4 MBLs have characteristically been associated with reactive conditions, most notably toxoplasma lymphadenitis 5 and h u m a n immunodeficiency virus (HlV)-associated lymphadenopathy. 6 In addition, MBL clusters have been noted rarely around Reed-Sternberg cells in Hodgkin's disease. 7 Lymphomas comprised of MBLs develop most commonly in adult patients with a history of autoimmune disease such as Sjogren's syndrome. 8-10 It has been suggested that the background of immune dysfunction may provide a predisposing substrate for subsequent development of lymphoma. MBCLs and low-grade lymphomas of mucosa-associated lymphoid tissue (MALT) share several common histologic, immunophenotypic, and clinical features, suggesting they are

From the Hematopathology Section, Laboratory of Pathology, National Cancer Institute, National Institutes of Health, Bethesda, Maryland. Manuscript received June 13, 1996; revision accepted August 14,1996. Address reprint requests to Dr Jaffe: Bldg 10, Rm 2N202, 10 Center Dr, MSC-1500, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892-1500.

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We report two cases of marginal zone B-cell lymphoma in two patients 6 and 18 years of age, respectively (cases 1 and 2) who had no clinical evidence of immunodeficiency or risk factors for human immunodeficiency virus (HIV) infection. Histologic analysis in both cases revealed diffuse nodal effacement by a monotonous population of atypical lymphoid cells with abundant pale cytoplasm and round to oval nuclei, with very infrequent mitotic activity. The neoplastic cells in both cases were of B-cell lineage (CD20 and CD79a positive), with CD43 coexpression. One case showed monoclonal light chain expression, and polymerase chain reaction analysis demonstrated clonal rearrangements of the immunoglobulin heavy chain gene in both cases. Abnormal cytogenetic findings were detected in case 2, in which metaphase

ELENITOBA-JOHNSON ET AL

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B-Cell Lymphoma With Monocytoid B-Cell Lymphocytes in Pediatric Patients

Surgical excision of a 3.0x2.4Xl.6-cm lymph node was performed in October 1995. At intraoperative consultation, frozen sections were preliminarily interpreted as atypical lymphoid hyperplasia. Immunofluorescence studies using antibodies against terminal deoxynucleotidyl transferase were negative. Tissue was submitted for routine histopathologic evaluation of permanent sections, immunohistochemistry, flow cytometry, gene rearrangement, and cytogenetic studies. MATERIALS AND METHODS Immunophenotypic

Immunohistochemical studies were performed with fixed paraffin-embedded sections and an avidinbiotin peroxidase complex technique, on an automated immunostainer (Ventana Medical System, Tucson), using monoclonal antibodies MB1 (CD79a) (gift from Dr David Mason), L26 (CD20), anti-CD3, anti-bc/-2, anti-IgK, anti-IgA. (Dako, Carpinteria, Calif), and Leu22 (CD43) (Becton Dickinson, San Jose, Calif). Cytogenetics

CASE REPORTS Case 1 In September 1995, a 6-year-old boy with an unremarkable medical history was noted by his mother to have a mass on the posterior neck, which progressively enlarged over 5 months. Physical examination by the family physician revealed no other masses, and the patient had no other symptoms. No evidence of congenital immunodeficiency or risk factors for acquired immunodeficiency (eg, HIV) were present in the child or documented in either parent. There was no e v i d e n c e of Toxoplasma infection. S e r u m i m m u n o g l o b u l i n s t u d i e s w e r e not p e r f o r m e d . Excisional biopsy of a 3.5X1 x0.7-cm lymph node was performed in October 1995, and tissue was submitted for flow cytometric studies.

Studies

Studies

Interphase cytogenetic analysis for trisomy 3 was performed using biotinylated a-satellite probes for chromosome 3 (D7Z1) (ONCOR, Gaithersburg, Md) according to published methods. 1 7 The slides were examined under oil immersion, and the signals per nucleus were counted for a minimum of 300 intact nuclei. Overlapping or indistinct nuclei were not included, and cases with more than 15% nuclei showing trisomy were scored as positive. 17 Karyotypic analysis by metaphase spreads was performed only in case 2. In Situ Hybridization

for Epstein-Barr Virus

In situ hybridization for EBV was performed on fixed p a r a f f i n - e m b e d d e d sections as p r e v i o u s l y described. 18

Case 2

Molecular Genetic Studies

An otherwise asymptomatic 18-year-old man with an unremarkable medical history had left submaxillary lymph node enlargement in September of 1995. No other peripheral lymphadenopathy was present. Serologic studies for Epstein-Barr virus (EBV) and toxoplasmosis yielded negative results. No risk factors for HIV infection were documented. Results of quantitative serum immunoglobulin studies were normal.

Genomic DNA was extracted from paraffin blocks from both cases using standard methods. This purified DNA was used to assay for clonal rearrangements of the immunoglobulin heavy chain (IgH) gene using a p o l y m e r a s e chain reaction (PCR) assay. 1 9 Paired oligonucleotide primers specific for the IgH gene joining region (5'-ACCTGAGGAGACGGTGACC-3') and the conserved framework three (FR3) segment of the

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related entities. 9 Indeed, in most cases MBCL appears to represent nodal involvement by an extranodal MALT l y m p h o m a . Both n e o p l a s m s h a v e been described synchronously and sequentially in the same patient,9'11 and it has been postulated that both tumors may share an identical histogenetic origin: a postgerminal center marginal zone B cell of extranodal or nodal type that retains the capacity to differentiate into plasma cells and monocytoid B cells.9,12 Thus, monocytoid B-cell lymphoma and low-grade B-cell lymphoma of MALT type have been designated nodal marginal zone B-cell lymphoma and extranodal marginal zone B-cell lymphoma, respectively.13 We recently reported two cases of p u l m o n a r y MALT lymphoma in children with HIV infection, 14 ' 15 and others have reported additional cases with similar features. 16 To our knowledge, neither MBCL nor MALT lymphomas have been reported in pediatric patients without immunodeficiency. In this report, we describe two cases of monocytoid B-cell lymphoma in young patients without evidence of immune dysfunction or HIV infection.

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To e v a l u a t e for the presence of the bc/-2/IgH chromosomal translocation t(14;18)(q32;q21), which is c h a r a c t e r i s t i c of follicular l y m p h o m a s , PCR a s s a y s a l s o w e r e p e r f o r m e d , as p r e v i o u s l y described. 2 0 Southern blot hybridization analysis was performed using molecular probes specific for the joining region of the i m m u n o g l o b u l i n heavy chain gene (JH) and immunoglobulin kappa light chain gene (IK). RESULTS A summary of the clinicopathologic and molecular findings in both patients is presented in the Table.

Pathologic

Findings

In case 1, a pink-tan 3.5X1 x0.7-cm lymph node was excised. Cross sections revealed a thin capsule and a light tan cut surface. Histologic sections revealed atypical lymphoid cells in a marginal zone pattern of distribution around hyperplastic lymphoid follicles, with focal areas of marked interfollicular expansion (Fig 1, A). The neoplastic cells exhibited small oval to reniform nuclei and abundant pale cytoplasm, frequently w i t h distinct cell b o r d e r s (see Fig 1, A, inset). Occasional large cells were present. Rare mitoses were identified in some neoplastic cells. In case 2, a 3.0X2.4Xl.7-cm l y m p h n o d e w a s excised. Cross sections revealed a homogeneous light tan a n d fleshy cut surface. H i s t o l o g i c a n a l y s i s revealed the nodal architecture was subtotally effaced by a population of small to medium lymphoid cells with abundant pale cytoplasm (Fig 2, A). Occasional large cells were noted. Also admixed were frequent plasma cells and histiocytes. Vague follicles rendered indistinct secondary to infiltration by neoplastic lymphoid cells were also evident. Mitotic activity was infrequent in the neoplastic cells. Immunophenotypic

Findings

The neoplastic cells in both cases showed strong immunoreactivity with L26 (CD20) (see Figs 1, B and 2, B) and MB1 (CD79a) and coexpression with Leu-22 (CD43) (see Fig 1, C) but were negative for anti-CD3. The intensity of staining observed in the Leu-22-positive neoplastic cells was less than that noted in the interfollicular background T cells. The ratio of IgK to Ig^. light chain expression was difficult to evaluate because of high background and interstitial staining.

CLINICOPATHOLOGIC AND GENETIC FINDINGS Gene Rearrangement Case No.

Age (y)

Sex M

1

18

M

Immunophenotype CD79a+, CD20+, CD43+, CD3-, bcl-2-, IgX CD79a+, CD20+, CD43+, CD3-, bcl-2-, TdT-

Cytogenetics In Situ Hybridization for Trisomy 3

In Situ

EBV Hybridization

VJ-PCR

bcl-2//H

SB

Karyotype

Clonal

Negative

ND

ND

Negative

Negative

Clonal

Negative

47,XY,+13

Negative

Negative

VJ-PCR = polymerase chain reaction (PCR) assay for clonal rearrangements of immunoglobulin heavy chain gene; bcl-2/]H = PCR for bcl-2/JH translocation; SB = Southern blot hybridization; EBV = Epstein-Barr virus; R = clonal rearrangements; TdT = terminal deoxynucleotidyl transferase; ND = not done.

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IgH gene v a r i a b l e r e g i o n s ( 5 ' - A C A C G G C [ C / T ] [G/C]TGTATTACTGT- 3') were used. In both cases, 1 ug of purified DNA was amplified in a 50 uL reaction containing PCR buffer ( G e n A m p ; P e r k i n Elmer, Norwalk, Conn), 1.5 mmol/L of magnesium chloride, four deoxy-nucleotide triphosphates at 200 umol/L, primers at 1 umol/L, and 1 unit of AmpliTaq DNA polymerase (Perkin Elmer). A hot start technique was used in all assays, with 35 cycles of denaturation (96°C for 1 m i n u t e ) , a n n e a l i n g (56°C for 1 minute), and extension (74°C for 1 minute). The PCR assays included polyclonal control (reactive lymph node), positive control (MBCL), and negative control (sample DNA omitted) reactions. PCR products were analyzed using standard polyacrylamide gel electrophoresis with molecular w e i g h t stand a r d s , stained with e t h i d i u m bromide, and p h o tographed under ultraviolet light. One or two dominant bands indicates the presence of a monoclonal B-cell population, whereas a polyclonal population results in either a smear or a ladder of b a n d s of nearly equivalent intensity.


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B-Cell Lymphoma With Monocytoid B-Cell Lymphocytes in Pediatric Patients

x

^'^2i^

However, admixed polyclonal plasma cells were identified. In both cases, bcl-2 protein was negative both in the follicular centers and in the neoplastic cells. MIB-1 contrasted the high proliferative activity present within the germinal centers with the low proliferative rate in the neoplastic lymphoid cells. In case 1, flow cytometric studies revealed a small population of B cells expressing monotypic IgL Molecular

Findings

Using PCR assays, we detected single dominant bands indicating the presence of clonal IgH rearrangements in both cases (Fig 3). Also, in case 2 Southern blot hybridization analysis performed at the referring institution, using a molecular probe specific for the

joining region of the immunoglobulin heavy chain gene (JH), revealed single rearranged bands with BamHI and EcoRl digestion and two rearranged bands with Hindlll digestion, indicative of monoclonal B-cell proliferation. The same assay using a probe specific for the joining region of the immunoglobulin K light chain showed rearranged bands after digestion by each of the three restriction enzymes. PCR assays to detect the presence of the bc/-2/IgH translocation were negative with appropriate controls (data not shown). Cytogenetic

Findings

In case 1, 10% of the cell nuclei showed one signal, 88% showed two signals, and 2% showed three signals.

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FIG 1. (Case 1) A, Cervical lymph node shows marginal zone, perifollicular pattern of involvement by MBCL (hematoxylin-eosin, X50). Inset, Cytologic detail of MBCL (hematoxylin-eosin, X630). B, Neoplastic cells show strong immunoreactivity with L26 (CD20) (avidin-biotin complex immunoperoxidase technique, X50). C, Atypical cells show Leu-22 (CD43) coexpression and exhibit less intense reactivity than do the surrounding reactive T cells, which show strong immunoreactivity for Leu-22 (avidin-biotin complex immunoperoxidase technique, X100).

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In case 2, 17% of cell nuclei showed one signal, 72% showed two signals, and 11% showed three signals. In both cases, fewer than 15% of the nuclei showed three signals and were thus scored as negative for the presence of trisomy 3. Of interest in case 2, classic cytogenetics studies p e r f o r m e d at the r e f e r r i n g i n s t i t u t i o n , u s i n g metaphase spreads, revealed the presence of trisomy 13 (karyotype 47,XY+13). In Situ

Leu-22 coexpression has been reported in association with the atypical lymphoid hyperplasia of infectious mononucleosis, 22 the neoplastic cells in our cases were negative for EBV by in situ hybridization, further validating the interpretation of Leu-22 coexpression as indicative of neoplasia. Monoclonality was confirmed

Hybridization

In situ hybridization for EBV was negative in both cases. DISCUSSION Both cases illustrate the histologic patterns typically seen in MBCL. In case 1, the neoplastic cells were distributed in a perifollicular (marginal zone) pattern around germinal centers (see Fig 1, A), with rare foci of follicular center colonization. In case 2, there was more diffuse effacement of nodal architecture by the neoplastic cells (see Fig 2, A). Immunohistochemical stains for IgK and IgX light chains were difficult to interpret because of high background and interstitial staining. As is commonly seen in MBCL, the atypical cells were bcl-2 negative by immunohistochemistry. Coexpression of Leu-22 (CD43) by the neoplastic cells in both cases supported an abnormal and possibly neoplastic phenotype (see Fig 1, C). 21 Although

FIG 3. Polymerase chain reaction analysis for immunoglobulin heavy rearrangements subjected to electrophoresis on 20% polyacrylamide gel with ethidium bromide staining. Clonal B-cell processes are identified as one or two dominant bands, and polyclonal processes as a smear or ladder of bands of equal intensity on ethidium bromide staining. M, size marker, in base pairs shown at left; lanes 1 and 4, known positive controls; lane 2, negative polyclonal control (human tonsil); lane 3, master mix control (no DNA added); lanes 7 and 8, dominant bands indicate clonal rearrangements of IgH gene in DNA extracted from paraffin blocks from cases 1 and 2, respectively.



FIG 2. (Case 2) A, Submaxillary lymph shows diffuse effacement by neoplastic monocytoid B cells with small to medium nuclei and abundant pale cytoplasm (hematoxylin-eosin, X400). B, Atypical cells show strong L26 (CD20) immunoreactivity (avidin-biotin complex immunoperoxidase technique, X400).


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B-Cell Lymphoma With Monocytoid B-i '.ell Lymphocytes in Pediatric Patients

Classic cytogenetic studies performed on fresh material obtained from case 2 revealed trisomy 13. Trisomy 13 has been reported in association with acute myeloid and lymphoid leukemias, myelodysplasia: syndrome, and chronic myeloid leukemia 2 5 but has not been documented in association with MBCL. Slovak et al 26 studied four cases of composite low-grade B-cell lymphoma in which MBCL was a substantial component, and identified a number of clonal cytogenetic abnormalities. One of their cases was characterized by an unbalanced 3;13 translocation involving band 13ql4, the locus of the retinoblastoma tumor suppressor gene. Some other findings in so-called composite MBCL have included t(ll;14) and t(14;18) translocations. These results suggest either m a n t l e cell l y m p h o m a or follicular l y m p h o m a , respectively, showing monocytoid B-cell differentiation within a single clone. These abnormalities have not been detected in primary or pure MBCL.

Low-grade B-cell lymphomas are exceedingly rare in children. Extranodal marginal zone B-cell lymphomas have been reported in the pediatric age group in association with HIV. Indeed, in both of our cases there was initial reluctance to make a diagnosis of lymphoma because of the young age of the patients and the partial architectural effacement. Therefore, it is important to recognize that marginal zone B-cell lymphomas can occur in this setting. Although most pediatric HIV-associated lymphomas are high-grade nonH o d g k i n ' s l y m p h o m a , w i t h a predilection for extra-nodal sites, 23 increasing numbers of MALT lymphomas are being reported in pediatric patients with HIV infection. 14-16 EBV infection, which occurs frequently in HIV-infected patients and has been implicated in the pathogenesis of many acquired immuno-deficiency-related high-grade B-cell non-Hodgkin's lymphomas, appears to have less pathogenetic significance in the low-grade B-cell lymphomas. 14,24 The association between MBCLs and low-grade Bcell lymphomas of MALT is well established. 8 ' 11 - 13 Cogliatti et al11 reported 21 cases of MBCL, and 7 of these patients had concomitant or subsequent lymphomas of MALT. Nizze et al 9 examined the draining lymph nodes from 58 gastric lymphomas of MALT type and found the pattern of MBCL in 10. MBCLs, also termed centrocyte-like cells, comprise a significant proportion of the neoplastic cells in many MALT lymphomas, particularly those with salivary gland involvement. These observations suggest that MBCL most often represents nodal involvement by a MALT lymphoma. However, neither of our patients had evidence of extranodal disease or involvement of mucosa.

The p a t h o g e n e t i c m e c h a n i s m s u n d e r l y i n g the development of these neoplasms in our patients is currently obscure. Both were negative for EBV and trisomy 3 by in situ hybridization. It is important to recognize and define this category of diseases to determine their relationship with MBCLs in adults or other low-grade B-cell lymphomas described in immunocompromised children, enabling comparison of clinical and biologic behavior and prognostic parameters.

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Acknowledgments: We t h a n k Drs M o h a m m e d Barudi and Richard K. Cochran, and Drs Errol Berman, Harvey Zimbler, and Emelie Ongcapin for providing clinical information and referral of patients 1 and 2, respectively.

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in both cases by PCR analysis, which demonstrated clonal rearrangements of the IgH (see Fig 3). MBCL is a low-grade lymphoma found in adults. In a series of 31 cases of MBCL studied by Ngan et al, 8 the age range of patients with MBCL was 29 to 85 years (median, 65 years). Similarly, Cogliatti et al 11 examined 21 patients with MBCL and reported ages ranging from 34 to 83 years (median, 59 years). In • most studies, the majority of the patients (>60%) had localized disease (clinical stage I or II). 8 ' 10 ' 11 In the series of Ngan et al, 8 of 36 patients (22%) had a history of Sjogren's syndrome, 1 of 36 (2.7%) had systemic lupus erythematosus, and 2 of 36 (5.5%) had monoclonal g a m m o p a t h y . The frequent association of MBCL with autoimmune diseases suggests a pathogenetic predisposition. Both of our patients were young (6 and 18 years old), and neither had any clinical or serologic evidence of autoimmune disease or congenital or acquired immunodeficiency.

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8. Ngan BY, Warnke RA, Wilson M, et al. Monocytoid B-cell lymphoma: a study of 36 cases. Hum Pathol. 1991;22:409-421. 9. Nizze H, Cogliatti SB, Von Schilling C, et al. Monocytoid B-cell lymphoma: morphological variants and relationship to lowgrade B-cell lymphoma of the mucosa-associated lymphoid tissue. Histopathologxj. 1991;18:403-414. 10. Shin S, Sheibani K, Fishleder A, et al. Monocytoid B-cell lymphoma in patients with Sjogren's syndrome: a clinicopathologic study of 13 patients. Hum Pathol. 1991; 22:422-430. 11. Cogliatti SB, Lennert K, Hansmann ML, Zwingers TL. Monocytoid B-cell lymphoma: clinical and prognostic features of 21 patients. / Clin Pathol. 1990;43:619-625. 12. Harris NL. Low-grade B-cell lymphoma of mucosa-associated lymphoid tissue and monocytoid B-cell lymphoma: related entities that are distinct from other low-grade B-cell lymphomas. Arch Pathol Lab Med. 1993;117:771-775. Editorial. 13. Harris NL, Jaffe ES, Stein H, et al. A revised EuropeanAmerican classification of lymphoid neoplasms: a proposal from the International Lymphoma Study group. Blood. 1994;84:1361-1392. 14. Teruya-Feldstein J, Temeck BK, Sloas MM, et al. Pulmonary malignant lymphoma of mucosa-associated lymphoid tissue (MALT) arising in a pediatric HIV-positive patient. Am ] Surg Pathol. 1995;19:357-363. 15. Teruya-Feldstein J, Temeck BK, Sloas MM, et al. Am J Surg Pathol. 1996;20:644. Letter. 16. Joshi B, Gagnon E, Chadwick, et al. Mucosal associated lymphoid tissue (MALT) lesions in pediatric patients infected with human immunodeficiency virus (HIV). Blood. 1995; 86:1507. Abstract.