CD5-Positive Follicular Lymphoma: A Case Report and Literature Review
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1 CASE REPORT CD5-Positive Follicular Lymphoma: A Case Report and Literature Review Yasunobu Sekiguchi 1, Hidenori Imai 1, Mutsumi Wakabayashi 1, Tomohiro Sawada 2, Kunimoto Ichikawa 3, Norio Komatsu 3 and Masaaki Noguchi 1 Abstract A 59-year-old man exhibited an enlarged right inguinal lymph node in February A pathological diagnosis of follicular lymphoma (FL), grade 3A, was made based on a biopsy specimen from the right inguinal lymph node. The immunophenotypes of the lymphoma cells were CD3-, CD5+, CD7-, CD10+, CD19+, CD20+, CD23+, IgM+, Igκ-, and Igλ+. Fluorescence-activated cell sorting (FACS) dual staining indicated that the cells were double-positive for both CD5 and CD20. Mantle cell lymphoma (MCL), small lymphocytic lymphoma (SLL) and CD5-positive diffuse large B-cell lymphoma (DLBCL) were ruled out by the presence of cyclin D1-, CD10+, and the pathological findings. Based on these findings, the patient was diagnosed as having CD5-positive FL. Eight cycles of rituximab plus six cycles of CHOP were performed, and complete remission was achieved. To our knowledge, this is a rare case of CD5-positive FL. A literature review suggested a relatively higher incidence in younger and male patients. Remarkably, patients with grade 3 tend to undergo a transformation from CD5-positive FL to DLBCL. Key words: CD5+, follicular lymphoma, grade 3A (Intern Med 50: , 2011) () Introduction Ninety-five percent of CD5 antigen occurs in thymocytes and immature peripheral T cells (1). A very small proportion of non-neoplastic CD5-positive B cells are also known to be present in peripheral blood and peripheral lymphoid tissues (1). These CD5-positive B cells constitute such disorders as small lymphocytic lymphoma (SLL), mantle cell lymphoma (MCL) or some of diffuse large B-cell lymphoma (DLBCL) when they undergo neoplastic transformation. CD5-positive DLBCL is generally recognized as a disease with an unfavorable prognosis (2), and as only a few reports on CD5-positive follicular lymphoma (FL) are available, its incidence and prognosis have not been completely understood. We recently encountered a case of CD5-positive, grade 3A FL. This report describes the present case and includes a review of previous documented in the literature. Case Report A 59-year-old man exhibited an enlargement of the right inguinal lymph node which developed in February 2009, and the patient was seen at the outpatient service of the Department of Surgery of this hospital during that month. A CT scan disclosed a few lymph nodes less than 1 cm in diameter in the axilla bilaterally and a right inguinal lymph node measuring 3.5 cm in diameter. A whole body gallium scintiscan revealed a slight bilateral accumulation in the axillae. A right inguinal lymph node biopsy was performed in April, and the condition was diagnosed as FL grade 3A; the patient was subsequently admitted to this hospital in May A few lymph nodes several mm in diameter were felt in the axilla bilaterally, and a lymph node as large as about 4 cm in diameter was palpable in the right inguinal region. No abnormalities were noted in the hematological tests, Division of Hematology, Juntendo University Urayasu Hospital, Japan, Division of Clinical Laboratory, Juntendo University Urayasu Hospital, Japan and Division of Hematology, Juntendo University Juntendo Hospital, Japan Received for publication August 7, 2010; Accepted for publication January 6, 2011 Correspondence to Dr. Yasunobu Sekiguchi, yasu_sek@juntendo-urayasu.jp 899
2 A B C D E F G H Figure 1. Histopathologic findings for right inguinal lymph node. A: Hematoxylin and Eosin staining ( 100); the basic architecture of the lymph node has been lost, and a follicle-like architecture were seen. B: Hematoxylin and Eosin staining ( 400); large centroblasts and relatively small centrocytes are intermingled, and it appeared to be a grade-3 FL. C: CD5 ( 600); the small strongly CD5- positive cells are T cells, and the weakly CD5-positive cells are FL. From small centrocytes to large centroblasts were seen, and these findings corresponded to grade 3A. D: CD10 ( 100); CD10 coincided with the follicle-like architecture and was positive. E: CD20 ( 100); CD20-positive cells were observed over a wide area, including the follicle-like architecture. F: Ki-67 ( 100); the high positive rate in the follicle-like architecture appeared to be attributable to the presence of numerous centroblasts. G: BCL2 ( 100); the follicle-like architecture was BCL2-negative, but because it can occur in grade-3a FL, there was no inconsistency. H: Cyclin D1 ( 100); staining was negative. blood biochemical tests, or urinalysis. Furthermore, no abnormalities were noted in immunoserological tests or the serum soluble IL-2 receptor level. A histopathologic examination of Hematoxylin and Eosin (H&E)-stained sections of a right inguinal lymph node biopsy specimen resulted in a diagnosis of FL grade 3A (Fig. 1A, 1B). Giemsa chromosome banding stain showed a complex abnormality with the 45,XY,-2,t(2;12)(p21;q24.1), +3,-8,der(9)t(9;21)(p11;q11.2),der(21)(21pter 21q21::2q?:: 8q22 8qter) (5 cells)/46,sl,+mar1 (2 cells)/47,sdl1,+r(8) (3 cells). Immunostained sections of the biopsy specimen proved to be weakly positive for CD5 (Fig. 1C), and positive for CD10 and CD20 (Fig. 1D, 1E). The MIB-1 index was moderate (Fig. 1F), and the specimen was negative for BCL2 and cyclin D1 (Fig. 1G, 1H). A flow cytometry analysis of the lymphoma cells in biopsied lymph node showed the following results: weak CD5+, CD10+, CD19+, CD20+, IgM+, and immunoglobulin light chains κ- and λ+ (Fig. 2A, 2C, 2D). The tissue was double-positive for CD5 and CD20 when examined using double staining (Fig. 2B). The case was diagnosed as being CD5-positive because flow cytometry is generally recognized as being superior to histopathological immunostaining with regard to CD5 sensitivity. A Southern blot analysis of the biopsy specimen revealed gene reconstitution of the immunoglobulin H chain (IgHJH) (Fig. 3A), while no gene reconstitution of the T cell receptor (TCR)Cβ1 chain was demonstrable (Fig. 3B); therefore, the lesion was considered to be a B cell tumor. Based on the above findings, a diagnosis of CD5-positive FL grade 3A was made. No BCL2 was demonstrated by fluorescence in situ hybridization (FISH) or by polymerase chain reaction (PCR), and Giemsa chromosome banding stain showed a complex abnormality with the absence of t(14;18)(q32;q21). 900
3 A B C D Figure 2. FACS dual staining using flow cytometry. A: Because of the λ predominance, it was considered to be a B-cell tumor. B: The strongly CD5-positive cells are normal cells, and the weakly CD5-positive, CD-20-positive cells are tumor cells. C: The tumor cells are CD10-positive. D: The tumor cells are IgM-positive, CD19-positive B cells. Negative control Specimen Negative control Specimen A B Figure 3. Southern blot assay. The restriction enzymes are: lane 1, EcoR I; lane 2, BamH I+Hind III; and lane 3, Hind III. A: Ig (H) JH, B: TCRCβ1, Red arrows show the rearranged bands in IgHJH assay. 901
4 Table 1. Thirty-six Reported Cases of CD5-positive FL Age/Sex Grade BCL2 Stage Transformation Treatment Outcome Survival Reference Time 75/F 3A NA IV none R-CHOP NA NA 4 40s/NA 1 + I DLBCL NA NA NA 5 50/M 3A + NA DLBCL MACOP- DOD 26m 6 B,ABMT 74/M 3B + III DLBCL COP, LEM, DOD 22m 6 CHOP, BLM 69/M 3B + IIE none CPA, MINE Surviving 14y 6 59/M 3A + NA DLBCL NA NA NA 6 57/F 3B + IV DLBCL R-CHOP, DOD 24m 6 ABMT 65/F 3B + IV DLBCL R-CHOP DOD 42m 6 57/F NA NA III none CHOP, Surviving 12y 7 CHOP-E, COP, R 49/F 1 NA IV none R-FDM Surviving NA 9 (CR) 52/M NA + NA none R-THPCOP Surviving NA 10 (CR) 32/M 1 + IV NA NA NA NA 12 55/F 2 + IV none NA NA NA 12 46/M 3A + I none NA NA NA 12 88/F NA + IV none RT NA NA 13 29/F 1 NA IV none NA Surviving 35m 14 46/M 2 NA IV none NA Surviving 42m 14 58/M 1 NA IV none NA DOD 50m 14 68/M 2 NA I none NA Surviving 15m 14 59/M 3A - III none R-CHOP Surviving 1y Present case NA:16 NA:16 III: 6 none: 6 (R)-CHOP: 6 NA: 16 NA: 16 8,11 +:10 -:6 NA:1 0 NA: 10 NA: 10 NA, not available; M, male; F, female; R, Rituximab; CHOP, cyclophosphamide, doxorubicin, vincristine, prednisolone; MACOP-B, methotrexate, doxorubicin, cyclophosphamide, vincristine, prednisolone; ABMT, allo bone marrow transplant; COP, cyclophosphamide, vincristine, prednisolone; LEM, liposome-entrapped mitoxantrone; BLM, bleomycin; CPA, cyclophosphamide; MINE, methotrexate, ifosfamide, mitoxantrone, etoposide; CHOP-E, cyclophosphamide, doxorubicin, vincristine, prednisolone, etoposide; FDM, fludarabine, dexamethasone, mitoxantrone; FL, follicular lymphoma; THP, pirarubicin; RT, radiation therapy; DLBCL, diffuse large B-cell lymphoma; DOD, died of disease; CR, complete remission; PR, partial remission; m, month; y, year However, this result is conceivable for FL grade 3 because about 50% of are negative for IgH-BCL2 and BCL2 proteins (3). As the present case was CD5-positive, the conditions that should be included in a differential diagnosis include MCL, SLL and CD5-positive DLBCL. The present case was negative for cyclin D1 and positive for CD 10 according to immunohistochemical staining (Fig. 1HD), and a FISH test did not reveal the presence of BCL1-IgH and BCL6; hence, MCL was ruled out. A diagnosis of SLL was also ruled out because no extrafollicular infiltration of CD10-positive cells was present (Fig. 1D). The patient was started on R-CHOP therapy because the condition was grade 3A, though low risk in terms of CSIIIA and FILIPI-1. The bilateral enlarged axillary lymph nodes and the enlarged right inguinal lymph node contracted, and the patient was discharged from hospital in June. A complete remission (CR) was achieved following a total of eight cycles of rituximab plus six cycles of CHOP therapy and has been maintained to date. Discussion CD5-positive FL is extremely rare, and its precise incidence is unknown. Only sporadic reports describing a total of 36 of CD5-positive FL, including the present case, have been made according to an extensive literature search (Table 1). The patients documented were relatively young, compared with reports on common FL (Table 2) (3). The condition was slightly more frequent among men. Grade 3 were more frequent, relative to common FL. The stage III and stage IV comprised a greater proportion of the reported, compared with the common FL. Transformation to DLBCL was confirmed in similar proportion. Of the patients with grade 1 or 2 CD5-positive FL, only 12.5% exhibited transformation. The showing transformation were of grade 3 disease 67% suggesting a relation- 902
5 Table 2. Comparison with FL, CD5 (+) FL and the Present Case CD5(-)FL CD5(+) FL Present case Mean age (yrs) 60s 56.4 (29-88) (n = 20) 59 Male/female 1:1.7 11:8 (n = 19) Male % of grade (9/17) Grade 3 Stage III or IV (%) (19/24) Stage III % with transformation (7/25) none Mean survival time (yrs) yrs (died: n = 5) 5.78 yrs (surviving: n = 6) Surviving for 1 yr % transformed at grade 1 or (1/8) % of transformed at grade (6/9) No transformation 4.12 yrs (died: n = 1) 7-10 grade 1 or 2 (yrs) 2.5 yrs (surviving: n = 3) 2.38 yrs (died: n = 4) 7-10 grade 3 (yrs) 7.5 yrs (surviving: n = 2) Surviving for 1 yr % of BCL2 positive at grade 1 or (3/3) % of BCL2 positive at grade (7/8) negative % of BCL2 positive at grade unknown NA 66.7(12/18) BCL2 Positive at grade 1 or 2 NA NA 2.38 yrs (died: n = 4) BCL2 NA positive at grade 3 14 yrs (surviving: n = 1) BCL2 negative at grade 3 NA 1 yr (surviving: n = 1) Surviving for 1 yr ship between grade 3 disease and transformation. The mean survival time was 5.78 years for the six currently surviving patients and 2.73 years for the five patients who died; thus, a poorer prognosis was observed among the latter. Focusing on grade 3, the mean survival time was 7.5 years for the 2 currently surviving patients and 2.38 years for the 4 patients who died, suggesting a poorer prognosis among the latter. The above findings suggest that the greater frequency of grade 3 disease and the higher percentage of transformed may account for the poorer prognosis of CD5-positive FL. The present case was also positive for CD10. Dong et al reported that lymphoma with the co-expression of CD5 and CD10 constituted about 0.4% of B cell type lymphoma, while FL accounted for 24% of those that were double-positive for CD5 and CD10 (11). Accordingly, FL that are both CD5- and CD10-positive are estimated to account for 0.096% of B cell lymphoma and thus are exceedingly rare. The expression of CD5 may occur in various other histologic types as well, and thus attention should focus on a differential diagnosis (12, 14). Why lymphoma cells become CD5-positive and why CD5-positive FL is rare remain unclear, and molecular biologic morphologic differences are yet to be clarified (5). Concomitant gene examination may be of value to a definite diagnosis. A consensus regarding prognosis has not been made, as one report has stated that the prognosis of CD5-positive FL does not differ from that of CD5- negative (8), while another report has stated that the prognosis was as unfavorable as that in CD5-positive DLBCL (5). As some reports suggest that CD5- positive FL may be liable to undergo transformation (5, 6), CD5-positive FL seems likely to have a poor prognosis, as may be inferred from the present summarization of 36 reported in which the grade 3 were frequently in a progressive phase and liable to show transformation with a shorter mean survival time. The results of BCL2 testing were available in 29, and the results of BCL2 according to grade were available in only 11. In grades 1 and 2, 100% of the were positive, and in grade 3, 87.5% were positive. The BCL2-positive rate tended to be higher in CD5-positive FL than in CD5-negative FL in every grade (Table 2). The results of BCL2 testing in relation to outcome were available in only 6 grade 3. The mean survival time of the 4 BCL2-positive patients who died was 2.38 years, and thus the prognosis appeared that is poor, and since there was only one BCL2-negative case, it was impossible to draw any conclusions about the prognosis. Further investigation is needed. The present findings also stress the importance of the careful monitoring of patients with grade 3 disease. Additional must be accumulated and compared with CD5-negative upon making a precise diagnosis including gene examination, BCL2 examination, clarification of the grade and stage of the disease at the time of diagnosis, and determination of whether the disease has undergone transformation and the clinical outcome to investigate the incidence of CD5-positive FL and to estimate its prognosis. 903
6 The authors state that they have no Conflict of Interest (COI). References 1. Chu PG, Chang KL, Arber DA, Weiss LM. Immunophenotyping of hematopoietic neoplasms. Semin Diagn Pathol 17: , Ennishi D, Takeuchi K, Yokoyama M, et al. CD5 expression is potentially predictive of poor outcome among biomarkers in patients with diffuse large B-cell lymphoma receiving rituximab plus CHOP therapy. Ann Oncol 19: , WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. 4th ed. Harris NL, Nathwani BN, Swerdlow SH, et al, Eds. IARC Press, Lyon, France, 2008: Ishiwata K, Ohta Y, Hasegawa E, Takagi S, Wake A, Ohashi K, Taniguchi S. A case of follicular lymphoma which was CD5(+) at initial examination and CD5(-) after recurrence. J Jpn Soc Lymphoreticular Tissue Res 48: 74, Vassallo J, Bousquet M, Quelen C, Al Saati T, Delsol G, Brousset P. CD5-positive diffuse large B cell lymphoma arising from a CD 5-positive follicular lymphoma. J Clin Pathol 60: , Manazza AD, Bonello L, Pagano M, et al. Follicular origin of a subset of CD5+ diffuse large B-cell lymphomas. Am J Clin Pathol 124: , Waki M, Kubota Y, Miyatani K, Ichimura K, Yoshino T, Nagai M. A case of CD10-negative, CD5-positive, low grade lymphoma with t(14;18) (q32;q21). Rinsho Ketsueki 46: 861, Kawano R, Karube K, Yamaguchi T, Ohshima K, Kikuchi M. A study on 6 of CD5-positive follicular large cell lymphoma. J Jpn Soc Lymphoreticular Tissue Res 44: 106, Kashimura M, Noro M, Akikusa B. A case of follicular lymphoma with leukemization of CD5 and CD20 double positive, CD23- positive lymphoma cells. J Jpn Soc Lymphoreticular Tissue Res 43: 71, Sato N, Takizawa A, Aoki S, Aizawa Y, Nakamura N. A case of follicular lymphoma with splenomegaly found in leukemic phase of CD5-positive, CD10-negative B cells. J Jpn Soc Lymphoreticular Tissue Res 43: 50, Dong HY, Gorczyca W, Liu Z, et al. B-cell lymphomas with coexpression of CD5 and CD10. Am J Clin Pathol 119: , Barry TS, Jaffe ES, Kingma DW, et al. CD5+ follicular lymphoma: a clinicopathologic study of three. Am J Clin Pathol 118: , Barekman CL, Aguilera NS, Abbondanzo SL. Low-grade B-cell lymphoma with coexpression of both CD5 and CD10. A report of 3. Arch Pathol Lab Med 125: , Tiesinga JJ, Wu CD, Inghirami G. CD5+ follicle center lymphoma. Immunophenotyping detects a unique subset of floral follicular lymphoma. Am J Clin Pathol 114: , Watanabe T. Follicular lymphoma. Saishin Igaku 59: , 2004 (in Japanese) The Japanese Society of Internal Medicine 904
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