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Coexisting well-differentiated and anaplastic thyroid carcinoma in the same primary resection specimen: immunophenotypic and genetic comparison of the two components in a consecutive series of 13 cases and a review of the literature

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Abstract

Anaplastic carcinoma (AC) is a rare but highly aggressive form of thyroid cancer. It mostly arises on a background of pre-existing well-differentiated cancer (WDC); however, whether it evolves directly from a WDC or originates as a second independent neoplasm is still to be defined. To obtain further insights into these mechanisms, we performed morphological, immunohistochemical, and next-generation sequencing analyses to compare AC and its associated WDC in a subset of 13 surgically resected specimens. Histologically, most WDC were of aggressive subtypes. Papillary carcinomas (8 cases; 62%) were tall cell (4/8), columnar (1/8), classic with hobnail features (1/8), classic and follicular variant in the remaining 2 cases; Hürthle cell and follicular carcinomas were present in 5 (38%) and in 1 (8%) patient, respectively. One patient harbored both a PTC, follicular variant, and a Hürthle cell carcinoma. We did not find any correlation between a histotype of WDC and a specific anaplastic growth pattern. Immunohistochemically, ACs retained pankeratin/PAX8 expression but with significantly lower levels than WDCs, and they tended to lose TTF1 expression, as can be expected within a dedifferentiation process. In addition, AC showed a more frequent expression of p63 and/or SMA, a mutated pattern of p53, and an abnormal expression of p16. Genetic analysis showed that the number of mutations was higher in AC than in the associated WDC, confirming a role of the progressive accumulation of genetic damage in this transition. We observed that mutations found in the WDCs were consistently identified in the anaplastic counterparts, further supporting the hypothesis of a developmental link.

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Contributions

Investigation: MR, SP, FT, BD, EK, DG, AF, and DdB. Data curation: MR, SP, FT, BD, AB, and EZ. Writing—original draft preparation: MR and SP. Writing—review and editing: AC. Supervision: GT. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the Italian Ministry of Health, grant number RF-2016-02364167.

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Authors and Affiliations

  1. Pathology Unit, Arcispedale Santa Maria Nuova, Azienda USL-IRCCS di Reggio Emilia, Viale Risorgimento 80, 42123, Reggio Emilia, Italy

    Moira Ragazzi, Eleonora Zanetti, Alessandra Bisagni & Simonetta Piana

  2. Laboratory of Translational Research, Arcispedale Santa Maria Nuova, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy

    Federica Torricelli, Benedetta Donati & Alessia Ciarrocchi

  3. Department of Pharmacy and Biotechnology, University of Bologna, Bologna, Italy

    Dario de Biase

  4. Molecular Diagnostic Unit, Department of Medicine (Dipartimento di Medicina Specialistica, Diagnostica e Sperimentale), Azienda USL di Bologna, University of Bologna, Bologna, Italy

    Giovanni Tallini

  5. Division of Pathology, Fondazione IRCCS Ca’ Granda, Ospedale Maggiore Policlinico, Department of Biomedical, Surgical, and Dental Sciences, University of Milan, Milan, Italy

    Elisabetta Kuhn

  6. Otolaryngology Unit, Arcispedale Santa Maria Nuova, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy

    Davide Giordano

  7. Endocrinology Unit, Arcispedale Santa Maria Nuova, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy

    Andrea Frasoldati

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  1. Moira Ragazzi
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Correspondence to Simonetta Piana.

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The study protocol was approved by the Institutional Review Board of the Azienda USL-IRCCS, Reggio Emilia, Italy (protocol no. 71141–2017).

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Ragazzi, M., Torricelli, F., Donati, B. et al. Coexisting well-differentiated and anaplastic thyroid carcinoma in the same primary resection specimen: immunophenotypic and genetic comparison of the two components in a consecutive series of 13 cases and a review of the literature. Virchows Arch 478, 265–281 (2021). https://doi.org/10.1007/s00428-020-02891-9

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