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Implications of SDHB genetic testing in patients with sporadic pheochromocytoma

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Abstract

Purpose

Succinate dehydrogenase B (SDHB) associated pheochromocytomas (PHEOs) are associated with a higher risk of tumor aggressiveness and malignancy. The aim of the present study was to evaluate (1) the frequency of germline SDHB mutations in apparently sporadic patients with PHEO who undergo preoperative genetic testing and (2) the ability to predict pathogenic mutations.

Methods

From 2012 to 2016, 82 patients underwent a PHEO surgical resection. Sixteen were operated in the context of hereditary PHEO and were excluded from analysis. Among the 66 remaining cases, 48 were preoperatively screened for an SDHB mutation. In addition to imaging studies with specific radiopharmaceuticals (123I-MIBG or 18F-FDOPA) for exclusion of multifocality/metastases, 36 patients underwent 18F-FDG PET/CT.

Results

From the 48 genetically screened patients, genetic testing found a germline SDHB variant in two (4.2%) cases: a variant of unknown significance, exon 1, c.14T>G (p.Val5Gly), and a most likely pathogenic mutation, exon 5, c.440A>G (p.Tyr147Cys), according to in silico analysis. Structural and functional analyses of the protein predicted that p.Tyr147Cys mutant was pathogenic. Both tumors exhibited moderate 18F-FDG PET uptake with similar uptake patterns to non-SDHB mutated PHEOs. The two patients underwent total laparoscopic adrenalectomies. Of the remaining patients, 44 underwent a laparoscopic adrenalectomy, and two had an open approach. Pathological analysis of the tumors from patients bearing two germline SDHB variants revealed a typical PHEO (PASS 0 and 2). Ex-vivo analyses (metabolomics, SDHB immunohistochemistry, loss of heterozygosity analysis) allowed a reclassification of the two SDHB variants as probably non-pathogenic variants.

Conclusions

This study illustrates that SDHx mutational analysis can be misleading, even if structural and functional analyses are done. Surgeons should be aware of the difficulty of classifying new SDHB variants prior to implementing SDHB mutation status into a tailored surgical management strategy of a patient.

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Authors’ contributions

Study conception and design: FS, DT, and KP. Acquisition of data: AM, CC, VJ, NCP, FS, and DT. Analysis and interpretation of data: EK, PR, AB, RCB, AI, DT, KP, WE, JM, and FS. Drafting of manuscript: DT, KP, AB, FS, FC, and AM. Critical revision of manuscript: DT, KP, FS, and FC.

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Authors and Affiliations

  1. Department of Endocrine Surgery, Conception Hospital, APHM, Aix Marseille Univ, Marseille, France

    Aurelie Maignan, Carole Guerin, Valentin Julliard, Nunzia-Cinzia Paladino & Fréderic Sebag

  2. Cancer Genetics, Kolling Institute of Medical Research, Royal North Shore Hospital, and University of Sydney, Sydney, New South Wales, Australia

    Edward Kim & Roderick Clifton-Bligh

  3. Integrative Structural & Chemical Biology (iSCB) & INT-3D Molecular Modeling Platform, Cancer Research Centre of Marseille, CNRS UMR7258, Aix Marseille Univ, Marseille, France

    Philippe Roche

  4. Department of Endocrinology, Conception Hospital, APHM, Aix Marseille Univ, Marseille, France

    Fréderic Castinetti

  5. Department of Neuropathology, La Timone University Hospital, APHM, Aix Marseille Univ, Marseille, France

    Wassim Essamet

  6. UMR_S912, IRD, Aix Marseille Univ, Marseille, France

    Julien Mancini

  7. ICube, UMR 7357 University of Strasbourg/CNRS and FMTS, Faculty of Medicine, Strasbourg, France

    Alessio Imperiale

  8. Laboratory of Biochemistry and Molecular Biology, Conception Hospital, APHM, Aix Marseille Univ, Marseille, France

    Pauline Romanet & Anne Barlier

  9. Section on Medical Neuroendocrinology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA

    Karel Pacak

  10. Department of Nuclear Medicine, La Timone University Hospital, APHM, CERIMED, Aix Marseille Univ, Marseille, France

    David Taïeb

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  1. Aurelie Maignan
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Correspondence to David Taïeb.

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The authors declare that they have no conflict of interest.

Research involving human participants

Data was acquired under regular clinical care conditions, with Ethics Committee approval obtained for the use of these data for scientific purposes.

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Written informed consent was obtained from all patients included in the present study.

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This research did not receive a specific grant from any funding agency in the public, commercial, or not-for-profit sector.

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Fréderic Sebag and David Taïeb contributed equally to this work

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Maignan, A., Guerin, C., Julliard, V. et al. Implications of SDHB genetic testing in patients with sporadic pheochromocytoma. Langenbecks Arch Surg 402, 787–798 (2017). https://doi.org/10.1007/s00423-017-1564-y

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