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01-09-2019 | Mantle Cell Lymphoma | Original Article

Inconsistency associated with SOX11 immunohistochemistry in mantle cell lymphoma: a meta-analysis

Authors: Woojoo Lee, Eun Shin, Bo Hyung Kim, Hyunchul Kim

Published in: Journal of Hematopathology | Issue 3/2019

Abstract

SOX11 immunohistochemistry (IHC) in mantle cell lymphoma (MCL) is known to show varied results. Our aim was to evaluate the factor responsible for this variation among different studies. A meta-analysis was performed with the original data including the proportion and number of SOX11-positive MCL cases, host and clonality of SOX11 antibodies, clone or catalog number of antibodies, MCL subtypes, number of cases with indolent traits, number of aggressive variants, and cut-off for SOX11 IHC interpretation. A total of 21 published studies were analyzed. The combined proportion of SOX11-positive MCL cases was 0.80 (95% CI = [0.72, 0.87]), and substantial heterogeneity was observed (I² = 83%). To explore sources of heterogeneity, subgroup analysis and meta-regression were done. Subgroup analysis with moderators of antibody clone or catalog number, antibody clonality, and monoclonal antibody clones showed substantial residual heterogeneity. Meta-regression with moderators of the proportion of cut-off value showed statistically significant result, although that with the aggressive cases did not. However, meta-regression with the cut-off value as a moderator showed substantial heterogeneity. The current meta-analysis of SOX11 immunohistochemistry in MCL showed the cut-off value to be important sources of overall heterogeneity.

Swerdlow SH (2017) WHO classification of tumours of haematopoietic and lymphoid tissues. World Health Organization classification of tumours, Revised fourth edition. International Agency for Research on Cancer. WHO Press, Lyon, France. Geneva, Switzerland

Mozos A, Royo C, Hartmann E, De Jong D, Baro C, Valera A, Fu K, Weisenburger DD, Delabie J, Chuang SS, Jaffe ES, Ruiz-Marcellan C, Dave S, Rimsza L, Braziel R, Gascoyne RD, Sole F, Lopez-Guillermo A, Colomer D, Staudt LM, Rosenwald A, Ott G, Jares P, Campo E (2009) SOX11 expression is highly specific for mantle cell lymphoma and identifies the cyclin D1-negative subtype. Haematologica 94(11):1555–1562. https://doi.org/10.3324/haematol.2009.010264 CrossRefPubMedPubMedCentral

Jay P, Goze C, Marsollier C, Taviaux S, Hardelin JP, Koopman P, Berta P (1995) The human SOX11 gene: cloning, chromosomal assignment and tissue expression. Genomics 29(2):541–545. https://doi.org/10.1006/geno.1995.9970 CrossRefPubMed

Ek S, Dictor M, Jerkeman M, Jirstrom K, Borrebaeck CA (2008) Nuclear expression of the non B-cell lineage Sox11 transcription factor identifies mantle cell lymphoma. Blood 111(2):800–805. https://doi.org/10.1182/blood-2007-06-093401 CrossRefPubMed

Lord M, Wasik AM, Christensson B, Sander B (2015) The utility of mRNA analysis in defining SOX11 expression levels in mantle cell lymphoma and reactive lymph nodes. Haematologica 100(9):e369–e372. https://doi.org/10.3324/haematol.2015.123885 CrossRefPubMedPubMedCentral

Zhang LN, Cao X, Lu TX, Fan L, Wang L, Xu J, Zhang R, Zou ZJ, Wu JZ, Li JY, Xu W (2013) Polyclonal antibody targeting SOX11 cannot differentiate mantle cell lymphoma from B-cell non-Hodgkin lymphomas. Am J Clin Pathol 140(6):795–800. https://doi.org/10.1309/AJCPEBOUJ7GVYVLG CrossRefPubMed

Kimura Y, Sato K, Imamura Y, Arakawa F, Kiyasu J, Takeuchi M, Miyoshi H, Yoshida M, Niino D, Sugita Y, Morito T, Yoshino T, Nakamura S, Ohshima K (2011) Small cell variant of mantle cell lymphoma is an indolent lymphoma characterized by bone marrow involvement, splenomegaly, and a low Ki-67 index. Cancer Sci 102(9):1734–1741. https://doi.org/10.1111/j.1349-7006.2011.01988.x CrossRefPubMed

Chen YH, Gao J, Fan G, Peterson LC (2010) Nuclear expression of sox11 is highly associated with mantle cell lymphoma but is independent of t(11;14)(q13;q32) in non-mantle cell B-cell neoplasms. Mod Pathol 23(1):105–112. https://doi.org/10.1038/modpathol.2009.140 CrossRefPubMed

Carvajal-Cuenca A, Sua LF, Silva NM, Pittaluga S, Royo C, Song JY, Sargent RL, Espinet B, Climent F, Jacobs SA, Delabie J, Naresh KN, Bagg A, Brousset P, Warnke RA, Serrano S, Harris NL, Swerdlow SH, Jaffe ES, Campo E (2012) In situ mantle cell lymphoma: clinical implications of an incidental finding with indolent clinical behavior. Haematologica 97(2):270–278. https://doi.org/10.3324/haematol.2011.052621 CrossRefPubMedPubMedCentral

10.

Chuang WY, Chang H, Chang GJ, Wang TH, Chang YS, Wang TH, Yeh CJ, Ueng SH, Chien HP, Chang CY, Wan YL, Hsueh C (2017) Pleomorphic mantle cell lymphoma morphologically mimicking diffuse large B cell lymphoma: common cyclin D1 negativity and a simple immunohistochemical algorithm to avoid the diagnostic pitfall. Histopathology 70(6):986–999. https://doi.org/10.1111/his.13161 CrossRefPubMed

11.

Gallo M, Cacheux V, Vincent L, Bret C, Tempier A, Guittard C, Mace A, Leventoux N, Costes V, Szablewski V (2016) Leukemic non-nodal mantle cell lymphomas have a distinct phenotype and are associated with deletion of PARP1 and 13q14. Virchows Archiv 469(6):697–706. https://doi.org/10.1007/s00428-016-2016-8 CrossRefPubMed

12.

Hsi AC, Hurley MY, Lee SJ, Rosman IS, Pang X, Gru A, Schaffer A (2016) Diagnostic utility of SOX11 immunohistochemistry in differentiating cutaneous spread of mantle cell lymphoma from primary cutaneous B-cell lymphomas. J Cutan Pathol 43(4):354–361. https://doi.org/10.1111/cup.12668 CrossRefPubMed

13.

Hsiao SC, Cortada IR, Colomo L, Ye H, Liu H, Kuo SY, Lin SH, Chang ST, Kuo TU, Campo E, Chuang SS (2012) SOX11 is useful in differentiating cyclin D1-positive diffuse large B-cell lymphoma from mantle cell lymphoma. Histopathology 61(4):685–693. https://doi.org/10.1111/j.1365-2559.2012.04260.x CrossRefPubMed

14.

Nakashima MO, Durkin L, Bodo J, Lin J, Quintanilla-Martinez L, Fu K, Hsi ED (2014) Utility and diagnostic pitfalls of SOX11 monoclonal antibodies in mantle cell lymphoma and other lymphoproliferative disorders. Appl Immunohistochem Mol Morphol 22(10):720–727. https://doi.org/10.1097/pai.0000000000000067 CrossRefPubMed

15.

O'Malley DP, Lee JP, Bellizzi AM (2017) Expression of LEF1 in mantle cell lymphoma. Ann Diagn Pathol 26:57–59. https://doi.org/10.1016/j.anndiagpath.2016.09.016 CrossRefPubMed

16.

Righi S, Pileri S, Agostinelli C, Bacci F, Spagnolo S, Sabattini E (2017) Reproducibility of SOX-11 detection in decalcified bone marrow tissue in mantle cell lymphoma patients. Hum Pathol 59:94–101. https://doi.org/10.1016/j.humpath.2016.09.018 CrossRefPubMed

17.

Roisman A, Huaman Garaicoa F, Metrebian F, Narbaitz M, Kohan D, Garcia Rivello H, Fernandez I, Pavlovsky A, Pavlovsky M, Hernandez L, Slavutsky I (2016) SOXC and MiR17–92 gene expression profiling defines two subgroups with different clinical outcome in mantle cell lymphoma. Genes Chromosom Cancer 55(6):531–540. https://doi.org/10.1002/gcc.22355 CrossRefPubMed

18.

Soldini D, Valera A, Sole C, Palomero J, Amador V, Martin-Subero JI, Ribera-Cortada I, Royo C, Salaverria I, Bea S, Gonzalvo E, Johannesson H, Herrera M, Colomo L, Martinez A, Campo E (2014) Assessment of SOX11 expression in routine lymphoma tissue sections: characterization of new monoclonal antibodies for diagnosis of mantle cell lymphoma. Am J Surg Pathol 38(1):86–93. https://doi.org/10.1097/PAS.0b013e3182a43996 CrossRefPubMed

19.

Zhang YH, Liu J, Dawlett M, Guo M, Sun X, Gong Y (2014) The role of SOX11 immunostaining in confirming the diagnosis of mantle cell lymphoma on fine-needle aspiration samples. Cancer Cytopathol 122(12):892–897. https://doi.org/10.1002/cncy.21465 CrossRefPubMed

20.

Hu Z, Sun Y, Schlette EJ, Tang G, Li S, Xu J, Yin CC, Young KH, Patel KP, Miranda RN, Goswami M, Wang M, Jorgensen JL, Medeiros LJ, Wang SA (2018) CD200 expression in mantle cell lymphoma identifies a unique subgroup of patients with frequent IGHV mutations, absence of SOX11 expression, and an indolent clinical course. Mod Pathol 31(2):327–336. https://doi.org/10.1038/modpathol.2017.135 CrossRefPubMed

21.

Abrisqueta P, Scott DW, Slack GW, Steidl C, Mottok A, Gascoyne RD, Connors JM, Sehn LH, Savage KJ, Gerrie AS, Villa D (2017) Observation as the initial management strategy in patients with mantle cell lymphoma. Ann Oncol 28(10):2489–2495. https://doi.org/10.1093/annonc/mdx333 CrossRefPubMed

22.

Gong Y, Zhang X, Chen R, Wei Y, Zou Z, Chen X (2017) Cytoplasmic expression of C-MYC protein is associated with risk stratification of mantle cell lymphoma. PeerJ 5:e3457. https://doi.org/10.7717/peerj.3457 CrossRefPubMedPubMedCentral

23.

Shih AR, Bledsoe JR, McKelvie P, Louissaint A, Harris NL, Zukerberg L (2017) CD5-negative mantle cell lymphoma shows a less aggressive outcome and variable SOX11 staining. J Hematop 10(2):49–53. https://doi.org/10.1007/s12308-017-0292-0 CrossRef

24.

Ondrejka SL, Lai R, Smith SD, Hsi ED (2011) Indolent mantle cell leukemia: a clinicopathological variant characterized by isolated lymphocytosis, interstitial bone marrow involvement, kappa light chain restriction, and good prognosis. Haematologica 96(8):1121–1127. https://doi.org/10.3324/haematol.2010.036277 CrossRefPubMedPubMedCentral

25.

Nordstrom L, Sernbo S, Eden P, Gronbaek K, Kolstad A, Raty R, Karjalainen ML, Geisler C, Ralfkiaer E, Sundstrom C, Laurell A, Delabie J, Ehinger M, Jerkeman M, Ek S (2014) SOX11 and TP53 add prognostic information to MIPI in a homogenously treated cohort of mantle cell lymphoma--a Nordic Lymphoma Group study. Br J Haematol 166(1):98–108. https://doi.org/10.1111/bjh.12854 CrossRefPubMedPubMedCentral

26.

Core Team R (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna

27.

Schwarzer G (2007) meta: an R package for meta-analysis. R News 7(3):40–45

28.

Deeks JJ, Higgins JPT, Altman DG (editors). Chapter 9: Analysing data and undertaking meta-analyses. In: Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 (updated March 2011). The Cochrane Collaboration, 2011. Available from https://www.handbook.cochrane.org. Retrieved 31 Jan 2019

29.

Thompson SG, Sharp SJ (1999) Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med 18(20):2693–2708CrossRefPubMed

30.

Nordstrom L, Andreasson U, Jerkeman M, Dictor M, Borrebaeck C, Ek S (2012) Expanded clinical and experimental use of SOX11 - using a monoclonal antibody. BMC Cancer 12:269. https://doi.org/10.1186/1471-2407-12-269 CrossRefPubMedPubMedCentral

31.

Fernandez V, Salamero O, Espinet B, Sole F, Royo C, Navarro A, Camacho F, Bea S, Hartmann E, Amador V, Hernandez L, Agostinelli C, Sargent RL, Rozman M, Aymerich M, Colomer D, Villamor N, Swerdlow SH, Pileri SA, Bosch F, Piris MA, Montserrat E, Ott G, Rosenwald A, Lopez-Guillermo A, Jares P, Serrano S, Campo E (2010) Genomic and gene expression profiling defines indolent forms of mantle cell lymphoma. Cancer Res 70(4):1408–1418. https://doi.org/10.1158/0008-5472.can-09-3419 CrossRefPubMed

32.

Zeng W, Fu K, Quintanilla-Fend L, Lim M, Ondrejka S, Hsi ED (2012) Cyclin D1-negative blastoid mantle cell lymphoma identified by SOX11 expression. Am J Surg Pathol 36(2):214–219. https://doi.org/10.1097/PAS.0b013e318241f050 CrossRefPubMed

33.

Wlodarska I, Dierickx D, Vanhentenrijk V, Van Roosbroeck K, Pospisilova H, Minnei F, Verhoef G, Thomas J, Vandenberghe P, De Wolf-Peeters C (2008) Translocations targeting CCND2, CCND3, and MYCN do occur in t(11;14)-negative mantle cell lymphomas. Blood 111(12):5683–5690. https://doi.org/10.1182/blood-2007-10-118794 CrossRefPubMed

34.

Salaverria I, Royo C, Carvajal-Cuenca A, Clot G, Navarro A, Valera A, Song JY, Woroniecka R, Rymkiewicz G, Klapper W, Hartmann EM, Sujobert P, Wlodarska I, Ferry JA, Gaulard P, Ott G, Rosenwald A, Lopez-Guillermo A, Quintanilla-Martinez L, Harris NL, Jaffe ES, Siebert R, Campo E, Bea S (2013) CCND2 rearrangements are the most frequent genetic events in cyclin D1(−) mantle cell lymphoma. Blood 121(8):1394–1402. https://doi.org/10.1182/blood-2012-08-452284 CrossRefPubMedPubMedCentral

35.

Cao X, Fan L, Fang C, Zhu DX, Dong HJ, Wang DM, Wang YH, Xu W, Li JY (2012) The expression of SOX11, cyclin D1, cyclin D2, and cyclin D3 in B-cell lymphocytic proliferative diseases. Med Oncol (Northwood, London, England) 29(2):1190–1196. https://doi.org/10.1007/s12032-011-9937-5 CrossRef

Title: Inconsistency associated with SOX11 immunohistochemistry in mantle cell lymphoma: a meta-analysis
Authors: Woojoo Lee
Eun Shin
Bo Hyung Kim
Hyunchul Kim
Publication date: 01-09-2019
Publisher: Springer Berlin Heidelberg
Keyword: Mantle Cell Lymphoma
Published in: Journal of Hematopathology / Issue 3/2019
Print ISSN: 1868-9256
Electronic ISSN: 1865-5785
DOI: https://doi.org/10.1007/s12308-019-00361-z

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Inconsistency associated with SOX11 immunohistochemistry in mantle cell lymphoma: a meta-analysis

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