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Is Immunohistochemical Staining for Β-Catenin the Definitive Pathological

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Is Immunohistochemical Staining for Β-Catenin the Definitive Pathological Human Pathology (2019) 84,155–163 www.elsevier.com/locate/humpath Original contribution Is immunohistochemical staining for β-catenin the definitive pathological diagnostic tool for desmoid-type fibromatosis? A multi-institutional study☆,☆☆ Hiroshi Koike MD a, Yoshihiro Nishida MD, PhD b,⁎, Kei Kohno MD, PhD c, Yoshie Shimoyama MD, PhD c, Toru Motoi MD, PhD d, Shunsuke Hamada MD, PhD e, Akira Kawai MD, PhD f, Akira Ogose MD, PhD g, Toshifumi Ozaki MD, PhD h, Toshiyuki Kunisada MD, PhD i, Yoshihiro Matsumoto MD, PhD j, Tomoya Matsunobu MD, PhD k, Keisuke Ae MD, PhD l, Tabu Gokita MD, PhD m, Tomohisa Sakai MD, PhD a, Koki Shimizu MD a, Naoki Ishiguro MD, PhD a aDepartment of Orthopedic Surgery, Nagoya University Graduate School of Medicine, Nagoya, Aichi 466-8550, Japan bDepartment of Rehabilitation, Nagoya University Hospital, Nagoya, Aichi 466-8550, Japan cDepartment of Pathology and Laboratory Medicine, Nagoya University Hospital, Nagoya, Aichi 466-8550, Japan dDepartment of Pathology, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo 113-8677, Japan eDepartment of Orthopedic Surgery, Aichi Cancer Center Hospital, Nagoya 464-8681, Japan fDepartment of Musculoskeletal Oncology, National Cancer Center Hospital, Tokyo 104-0045, Japan gDepartment of Orthopedic Surgery, Uonuma Institute of Community Medicine, Niigata University Medical and Dental Hospital, Niigata 949-7302, Japan hDepartment of Orthopedic Surgery, Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama 700-8558, Japan iDepartment of Medical Materials for Musculoskeletal Reconstruction, Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama 700-8558, Japan jDepartment of Orthopedic Surgery, Kyushu University, Fukuoka 812-8582, Japan kDepartment of Orthopedic Surgery, Kyushu Rosai Hospital, Fukuoka 800-0296, Japan lDepartment of Orthopedic Surgery, Cancer Institute Hospital, Japanese Foundation for Cancer Research, Tokyo 135-8550, Japan mDepartment of Orthopedic Surgery, Saitama Cancer Center, Saitama 362-0806, Japan Received 6 June 2018; revised 19 September 2018; accepted 26 September 2018 ☆ Competing interests: None. ☆☆ Funding/Support: This work was supported in part by the Ministry of Health, Labor and Welfare of Japan, and the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grant-in-Aid 17H01585 for Scientific Research [A]), and the National Cancer Center Research and Development Fund (29-A-3). ⁎ Corresponding author. E-mail address: [email protected] (Y. Nishida). https://doi.org/10.1016/j.humpath.2018.09.018 0046-8177/© 2018 Elsevier Inc. All rights reserved. 156 H. Koike et al. Keywords: Summary Immunohistochemical staining with anti–β-catenin antibody has been applied as a diagnostic tool Desmoid-type for desmoid-type fibromatoses (DFs). In recent years, specificgenemutation(CTNNB1) analysis has also fibromatosis; been reported to be useful for diagnosis of DF; however, the association between CTNNB1 mutation status β-Catenin; and immunohistochemical staining pattern of β-catenin is rarely reported. The purposes of this study are to Immunohistochemical clarify the relationship of the staining pattern of β-catenin with the CTNNB1 mutation status and various staining; clinical variables, and to investigate the significance of immunohistochemical staining of β-catenin in cases CTNNB1 mutation; diagnosed as DF. Between 1997 and 2017, 104 cases diagnosed as DF from 6 institutions in Japan were Multi-institutional study enrolled in this study: Nagoya University, National Cancer Center Hospital, Niigata University, Okayama University, Kyushu University, and Cancer Institute Hospital. For all cases, immunohistochemical staining of β-catenin and gene mutation analysis of CTNNB1 were performed. Of 104 cases, 87 (84%) showed nuclear staining of β-catenin, and 95 (91%) showed positive staining in the cytoplasm. The proportion of cases showing strong nuclear staining of β-catenin was significantly higher in the cases with S45F than in those with T41A or wild type. The proportion of cases stained strongly in the cytoplasm rather than in the nucleus was significantly higher in the group of T41A than that of S45F or wild type. Among 17 cases in which nuclear immunostaining was absent, CTNNB1 mutation was observed in 5 cases (29.4%). There were unignorable cases of DF with negative β-catenin immunostaining despite a definitive clinical and pathological diagnosis of DF and/or positive CTNNB1 mutation. © 2018 Elsevier Inc. All rights reserved. 1. Introduction few reports demonstrated the correlation between immunohis- tochemical staining pattern of β-catenin and CTNNB1 muta- Desmoid-type fibromatoses (DFs) are soft tissue tumors with tion status. clonal origin and mesenchymal fibroblastic/myofibroblastic In the present study, we aimed to clarify the association β proliferation, with an incidence of 2 to 4 cases per million between staining pattern of -catenin, patient characteristics, fi persons per year [1]. Most cases develop sporadically in adults, and CTNNB1 mutation status and assess the signi cance whereas a few occur against a family background of familial of immunohistochemical staining for nuclear or cytoplasmic β adenomatous polyposis [2]. DFs are generally highly invasive -catenin in 104 sporadic DF cases. and locally aggressive, but do not metastasize [3,4], and are categorized as intermediate tumors in the World Health Orga- nization classification [5]. Somatic mutations at exon 3 of CTNNB1 gene have been 2. Materials and methods reported as a molecular pathogenesis of sporadic DF. The mu- tation generally occurs at codon 41 or 45. These mutations in- 2.1. Tissue samples hibit phosphorylation of β-catenin, which protect β-catenin from degradation by adenomatous polyposis coli complex, This study has been performed according to the Declaration resulting in nuclear accumulation of β-catenin and activation of Helsinki, and ethical approval from the appropriate commit- of the T-cell factor/lymphoid enhancer factor pathway [6]. tees of Nagoya University was obtained for this study. A recent study showed that CTNNB1 mutations were Formalin-fixed, paraffin-embedded specimens accumulated highly prevalent and detected in 88% of sporadic DFs in between 1994 and 2017 were retrieved from 6 institutions: contrast to no hotspot CTNNB1 mutations in any of the spindle Nagoya University, National Cancer Center Hospital, Niigata cell nondesmoid lesions [7]. The hotspot mutation of CTNNB1 University, Okayama University, Kyushu University, and is thought to be very specific for DF. Recent studies exhibited Cancer Institute Hospital. There were 113 cases diagnosed as that tumors with CTNNB1 S45F mutation were reported to ex- sporadic DF. To confirm the histologic diagnosis of DF, sec- hibit resistance to surgical and conservative treatment [8,9], tions of all cases were transmitted to the Pathology Laboratory suggesting that CTNNB1 mutation analysis might be important at Tokyo Metropolitan Cancer and Infectious Diseases Center not only for the diagnosis of DF but also for determining the sub- Komagome Hospital for central pathology review (T. M.). sequent treatment options. However, CTNNB1 mutation analysis Based on the evaluation of central review and careful is performed only in limited facilities in Japan and has not yet discussion between the pathologist and physicians, 9 cases been generally applied for clinical use as a diagnostic tool, were excluded. No cases with an obvious history of familial whereas immunohistochemical staining of β-catenin has been adenomatous polyposis were included. Finally, this study considered useful for the diagnosis of DF [6,10-16]. These stud- was composed of 104 cases of DF. Specimens obtained ies investigated the significance of immunohistochemical staining by biopsy or surgical excision were formalin fixed and of β-catenin or CTNNB1 mutation status independently, and paraffin embedded, and subjected to examination of Significance of β-catenin staining for desmoid 157 Fig. 1 Representative images of immunohistochemical staining for β-catenin (original magnification ×200). Differential staining positivity of the nucleus and cytoplasm. Staining positivity: absent in the nucleus (A) and cytoplasm (B), weak in the nucleus (C) and cytoplasm (D), moderate in the nucleus (E) and cytoplasm (F), and strong in the nucleus (G) and cytoplasm (H). immunohistochemistry for β-catenin and CTNNB1 mutation Preparation Kit (Roche Molecular Diagnostics, Mannheim, analysis. The following clinical data were collected: age at Germany) according to the manufacturer's protocol. Extracted the diagnosis, gender, tumor location, and tumor size. DNA was amplified by polymerase chain reaction using LightCycler 480 System (Roche). To analyze the point 2.2. Mutation analysis mutations in codon 41 or 45 of CTNNB1 exon 3, we designed 2 pairs of primers: forward 59-GATTTGATGGAGTTGGA DNA was extracted from frozen tissue or formalin-fixed, CATGG-39, reverse 59-TCTTCCTCAGGATTGCCTT-39, paraffin-embedded tissue with the High Pure PCR Template and forward 59-TGGAACCAGACAGAAAAGCG-39, reverse 158 H. Koike et al. Fig. 2 Representative images of ×400 magnification. Staining intensity: absent in the nucleus (A) and cytoplasm (B), weak in the nucleus (C) and cytoplasm (D), moderate in the nucleus (E) and cytoplasm (F), and strong in the nucleus (G) and cytoplasm (H). 59-TCAGGATTGCCTTTACCACTC-39. Polymerase chain 2.3. Immunohistochemistry reaction products were isolated
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