Management of phaeochromocytoma and paraganglioma in patients with germline SDHB pathogenic variants: an international expert Consensus statement.

Journal

Nature reviews. Endocrinology
ISSN: 1759-5037
Titre abrégé: Nat Rev Endocrinol
Pays: England
ID NLM: 101500078

Informations de publication

Date de publication:
14 Dec 2023
Historique:
accepted: 16 11 2023
medline: 15 12 2023
pubmed: 15 12 2023
entrez: 14 12 2023
Statut: aheadofprint

Résumé

Adult and paediatric patients with pathogenic variants in the gene encoding succinate dehydrogenase (SDH) subunit B (SDHB) often have locally aggressive, recurrent or metastatic phaeochromocytomas and paragangliomas (PPGLs). Furthermore, SDHB PPGLs have the highest rates of disease-specific morbidity and mortality compared with other hereditary PPGLs. PPGLs with SDHB pathogenic variants are often less differentiated and do not produce substantial amounts of catecholamines (in some patients, they produce only dopamine) compared with other hereditary subtypes, which enables these tumours to grow subclinically for a long time. In addition, SDHB pathogenic variants support tumour growth through high levels of the oncometabolite succinate and other mechanisms related to cancer initiation and progression. As a result, pseudohypoxia and upregulation of genes related to the hypoxia signalling pathway occur, promoting the growth, migration, invasiveness and metastasis of cancer cells. These factors, along with a high rate of metastasis, support early surgical intervention and total resection of PPGLs, regardless of the tumour size. The treatment of metastases is challenging and relies on either local or systemic therapies, or sometimes both. This Consensus statement should help guide clinicians in the diagnosis and management of patients with SDHB PPGLs.

Identifiants

DOI: 10.1038/s41574-023-00926-0 PMID: 38097671
pubmed: 38097671
doi: 10.1038/s41574-023-00926-0
pii: 10.1038/s41574-023-00926-0
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.

Références

Kastriti, M. E. et al. Schwann cell precursors generate the majority of chromaffin cells in zuckerkandl organ and some sympathetic neurons in paraganglia. Front. Mol. Neurosci. 12, 6 (2019).
pubmed: 30740044 pmcid: 6355685 doi: 10.3389/fnmol.2019.00006
Furlan, A. et al. Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla. Science 357, eaal3753 (2017).
pubmed: 28684471 pmcid: 6013038 doi: 10.1126/science.aal3753
Baysal, B. E. et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287, 848–851 (2000).
pubmed: 10657297 doi: 10.1126/science.287.5454.848
Astuti, D. et al. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am. J. Hum. Genet. 69, 49–54 (2001).
pubmed: 11404820 pmcid: 1226047 doi: 10.1086/321282
Niemann, S. & Muller, U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat. Genet. 26, 268–270 (2000).
pubmed: 11062460 doi: 10.1038/81551
Burnichon, N. et al. SDHA is a tumor suppressor gene causing paraganglioma. Hum. Mol. Genet. 19, 3011–3020 (2010).
pubmed: 20484225 pmcid: 2901140 doi: 10.1093/hmg/ddq206
Andrews, K. A. et al. Tumour risks and genotype-phenotype correlations associated with germline variants in succinate dehydrogenase subunit genes SDHB, SDHC and SDHD. J. Med. Genet. 55, 384–394 (2018).
pubmed: 29386252 doi: 10.1136/jmedgenet-2017-105127
Richards, S. et al. Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet. Med. 17, 405–424 (2015).
pubmed: 25741868 pmcid: 4544753 doi: 10.1038/gim.2015.30
Lenders, J. W. et al. Pheochromocytoma and paraganglioma: an Endocrine Society clinical practice guideline. J. Clin. Endocrinol. Metab. 99, 1915–1942 (2014).
pubmed: 24893135 doi: 10.1210/jc.2014-1498
Taieb, D. et al. Current approaches and recent developments in the management of head and neck paragangliomas. Endocr. Rev. 35, 795–819 (2014).
pubmed: 25033281 pmcid: 4167435 doi: 10.1210/er.2014-1026
Gimenez-Roqueplo, A. P. et al. Imaging work-up for screening of paraganglioma and pheochromocytoma in SDHx mutation carriers: a multicenter prospective study from the PGL.EVA Investigators. J. Clin. Endocrinol. Metab. 98, E162–E173 (2013).
pubmed: 23162105 doi: 10.1210/jc.2012-2975
Assadipour, Y. et al. SDHB mutation status and tumor size but not tumor grade are important predictors of clinical outcome in pheochromocytoma and abdominal paraganglioma. Surgery 161, 230–239 (2017).
pubmed: 27839933 doi: 10.1016/j.surg.2016.05.050
Timmers, H. J. et al. Staging and functional characterization of pheochromocytoma and paraganglioma by
pubmed: 22517990 pmcid: 3341309 doi: 10.1093/jnci/djs188
Turkova, H. et al. Characteristics and outcomes of metastatic SDHB and sporadic pheochromocytoma/paraganglioma: an National Institutes of Health Study. Endocr. Pract. 22, 302–314 (2016).
pubmed: 26523625 doi: 10.4158/EP15725.OR
Gimenez-Roqueplo, A. P. et al. Functional consequences of a SDHB gene mutation in an apparently sporadic pheochromocytoma. J. Clin. Endocrinol. Metab. 87, 4771–4774 (2002).
pubmed: 12364472 doi: 10.1210/jc.2002-020525
Gimenez-Roqueplo, A. P. et al. Mutations in the SDHB gene are associated with extra-adrenal and/or malignant phaeochromocytomas. Cancer Res. 63, 5615–5621 (2003).
pubmed: 14500403
Schovanek, J. et al. The size of the primary tumor and age at initial diagnosis are independent predictors of the metastatic behavior and survival of patients with SDHB-related pheochromocytoma and paraganglioma: a retrospective cohort study. BMC Cancer 14, 523 (2014).
pubmed: 25048685 pmcid: 4223758 doi: 10.1186/1471-2407-14-523
Brouwers, F. M. et al. High frequency of SDHB germline mutations in patients with malignant catecholamine-producing paragangliomas: implications for genetic testing. J. Clin. Endocrinol. Metab. 91, 4505–4509 (2006).
pubmed: 16912137 doi: 10.1210/jc.2006-0423
Pamporaki, C. et al. Prediction of metastatic pheochromocytoma and paraganglioma: a machine learning modelling study using data from a cross-sectional cohort. Lancet Digit. Health 5, e551–e559 (2023).
pubmed: 37474439 doi: 10.1016/S2589-7500(23)00094-8
Rijken, J. A. et al. Increased mortality in SDHB but not in SDHD pathogenic variant carriers. Cancers 11, 103 (2019).
pubmed: 30658386 pmcid: 6356820 doi: 10.3390/cancers11010103
Papathomas, T. G. et al. Non-pheochromocytoma (PCC)/paraganglioma (PGL) tumors in patients with succinate dehydrogenase-related PCC-PGL syndromes: a clinicopathological and molecular analysis. Eur. J. Endocrinol. 170, 1–12 (2013).
pubmed: 24096523 doi: 10.1530/EJE-13-0623
Pasini, B. et al. Clinical and molecular genetics of patients with the Carney-Stratakis syndrome and germline mutations of the genes coding for the succinate dehydrogenase subunits SDHB, SDHC, and SDHD. Eur. J. Hum. Genet. 16, 79–88 (2008).
pubmed: 17667967 doi: 10.1038/sj.ejhg.5201904
Denes, J. et al. Heterogeneous genetic background of the association of pheochromocytoma/paraganglioma and pituitary adenoma: results from a large patient cohort. J. Clin. Endocrinol. Metab. 100, E531–E541 (2015).
pubmed: 25494863 doi: 10.1210/jc.2014-3399
Eisenhofer, G. et al. Catecholamine metabolomic and secretory phenotypes in phaeochromocytoma. Endocr. Relat. Cancer 18, 97–111 (2011).
pubmed: 21051559 doi: 10.1677/ERC-10-0211
Amar, L. et al. International consensus on initial screening and follow-up of asymptomatic SDHx mutation carriers. Nat. Rev. Endocrinol. 17, 435–444 (2021).
pubmed: 34021277 pmcid: 8205850 doi: 10.1038/s41574-021-00492-3
Atkins, D. et al. Grading quality of evidence and strength of recommendations. BMJ 328, 1490 (2004).
pubmed: 15205295 doi: 10.1136/bmj.328.7454.1490
Lenders, J. W. M. et al. Genetics, diagnosis, management and future directions of research of phaeochromocytoma and paraganglioma: a position statement and consensus of the Working Group on Endocrine Hypertension of the European Society of Hypertension. J. Hypertens. 38, 1443–1456 (2020).
pubmed: 32412940 pmcid: 7486815 doi: 10.1097/HJH.0000000000002438
Ben Aim, L. et al. International initiative for a curated SDHB variant database improving the diagnosis of hereditary paraganglioma and pheochromocytoma. J. Med. Genet. 59, 785–792 (2022).
pubmed: 34452955 doi: 10.1136/jmedgenet-2020-107652
Benn, D. E. et al. Bayesian approach to determining penetrance of pathogenic SDH variants. J. Med. Genet. 55, 729–734 (2018).
pubmed: 30201732 doi: 10.1136/jmedgenet-2018-105427
Daniel, E., Jones, R., Bull, M. & Newell-Price, J. Rapid-sequence MRI for long-term surveillance for paraganglioma and phaeochromocytoma in patients with succinate dehydrogenase mutations. Eur. J. Endocrinol. 175, 561–570 (2016).
pubmed: 27634942 doi: 10.1530/EJE-16-0595
Eijkelenkamp, K. et al. Calculating the optimal surveillance for head and neck paraganglioma in SDHB-mutation carriers. Fam. Cancer 16, 123–130 (2017).
pubmed: 27573198 doi: 10.1007/s10689-016-9923-3
Jafri, M. et al. Evaluation of SDHB, SDHD and VHL gene susceptibility testing in the assessment of individuals with non-syndromic phaeochromocytoma, paraganglioma and head and neck paraganglioma. Clin. Endocrinol. 78, 898–906 (2013).
doi: 10.1111/cen.12074
Jasperson, K. W. et al. Role of rapid sequence whole-body MRI screening in SDH-associated hereditary paraganglioma families. Fam. Cancer 13, 257–265 (2014).
pubmed: 23934599 doi: 10.1007/s10689-013-9639-6
Jochmanova, I. et al. SDHB-related pheochromocytoma and paraganglioma penetrance and genotype-phenotype correlations. J. Cancer Res. Clin. Oncol. 143, 1421–1435 (2017).
pubmed: 28374168 pmcid: 5505780 doi: 10.1007/s00432-017-2397-3
Martins, R. G. et al. Surveillance of succinate dehydrogenase gene mutation carriers: insights from a nationwide cohort. Clin. Endocrinol. 92, 545–553 (2020).
doi: 10.1111/cen.14184
Niemeijer, N. D. et al. The phenotype of SDHB germline mutation carriers: a nationwide study. Eur. J. Endocrinol. 177, 115–125 (2017).
pubmed: 28490599 doi: 10.1530/EJE-17-0074
Tufton, N., Sahdev, A. & Akker, S. A. Radiological surveillance screening in asymptomatic succinate dehydrogenase mutation carriers. J. Endocr. Soc. 1, 897–907 (2017).
pubmed: 29264540 pmcid: 5686572 doi: 10.1210/js.2017-00230
Tufton, N., Sahdev, A., Drake, W. M. & Akker, S. A. Can subunit-specific phenotypes guide surveillance imaging decisions in asymptomatic SDH mutation carriers? Clin. Endocrinol. 90, 31–46 (2019).
doi: 10.1111/cen.13877
Benn, D. E., Richardson, A. L., Marsh, D. J. & Robinson, B. G. Genetic testing in pheochromocytoma- and paraganglioma-associated syndromes. Ann. N. Y. Acad. Sci. 1073, 104–111 (2006).
pubmed: 17102077 doi: 10.1196/annals.1353.011
Eisenhofer, G. et al. Biochemical diagnosis of chromaffin cell tumors in patients at high and low risk of disease: plasma versus urinary free or deconjugated o-methylated catecholamine metabolites. Clin. Chem. 64, 1646–1656 (2018).
pubmed: 30097498 doi: 10.1373/clinchem.2018.291369
Eisenhofer, G. et al. Plasma methoxytyramine: a novel biomarker of metastatic pheochromocytoma and paraganglioma in relation to established risk factors of tumour size, location and SDHB mutation status. Eur. J. Cancer 48, 1739–1749 (2012).
pubmed: 22036874 doi: 10.1016/j.ejca.2011.07.016
Saie, C. et al. Screening of a large cohort of asymptomatic SDHx mutation carriers in routine practice. J. Clin. Endocrinol. Metab. 106, e1301–e1315 (2021).
pubmed: 33247927 doi: 10.1210/clinem/dgaa888
Rao, D. et al. Plasma methoxytyramine: clinical utility with metanephrines for diagnosis of pheochromocytoma and paraganglioma. Eur. J. Endocrinol. 177, 103–113 (2017).
pubmed: 28476870 pmcid: 5488393 doi: 10.1530/EJE-17-0077
Tufton, N., White, G., Drake, W. M., Sahdev, A. & Akker, S. A. Diffusion-weighted imaging (DWI) highlights SDHB-related tumours: a pilot study. Clin. Endocrinol. 91, 104–109 (2019).
doi: 10.1111/cen.13980
Gravel, G. et al. The value of a rapid contrast-enhanced angio-MRI protocol in the detection of head and neck paragangliomas in SDHx mutations carriers: a retrospective study on behalf of the PGL.EVA investigators. Eur. Radiol. 26, 1696–1704 (2016).
pubmed: 26427697 doi: 10.1007/s00330-015-4024-5
Janssen, I. et al. Superiority of [
pubmed: 25873086 pmcid: 4558308 doi: 10.1158/1078-0432.CCR-14-2751
Taieb, D. et al. European Association of Nuclear Medicine practice guideline/Society of Nuclear Medicine and Molecular Imaging procedure standard 2019 for radionuclide imaging of phaeochromocytoma and paraganglioma. Eur. J. Nucl. Med. Mol. Imaging 46, 2112–2137 (2019).
pubmed: 31254038 pmcid: 7446938 doi: 10.1007/s00259-019-04398-1
Carrasquillo, J. A. et al. Imaging of pheochromocytoma and paraganglioma. J. Nucl. Med. 62, 1033–1042 (2021).
pubmed: 34330739 pmcid: 8833868 doi: 10.2967/jnumed.120.259689
Kong, G. et al. The role of
pubmed: 30977831 doi: 10.1210/jc.2019-00018
Jha, A. et al. Superiority of
pubmed: 29204718 doi: 10.1007/s00259-017-3896-9
Buffet, A. et al. Positive impact of genetic test on the management and outcome of patients with paraganglioma and/or pheochromocytoma. J. Clin. Endocrinol. Metab. 104, 1109–1118 (2019).
pubmed: 30698717 doi: 10.1210/jc.2018-02411
Davidoff, D. F. et al. Surveillance improves outcomes for carriers of SDHB pathogenic variants: a multicenter study. J. Clin. Endocrinol. Metab. 107, e1907–e1916 (2022).
pubmed: 35037935 pmcid: 9016424 doi: 10.1210/clinem/dgac019
Raygada, M., King, K. S., Adams, K. T., Stratakis, C. A. & Pacak, K. Counseling patients with succinate dehydrogenase subunit defects: genetics, preventive guidelines, and dealing with uncertainty. J. Pediatr. Endocrinol. Metab. 27, 837–844 (2014).
pubmed: 24854530 pmcid: 4718145 doi: 10.1515/jpem-2013-0369
Athens, B. A. et al. A systematic review of randomized controlled trials to assess outcomes of genetic counseling. J. Genet. Couns. 26, 902–933 (2017).
pubmed: 28255928 pmcid: 7350655 doi: 10.1007/s10897-017-0082-y
Yip, L. et al. American Association of Endocrine Surgeons guidelines for adrenalectomy: executive summary. JAMA Surg. 157, 870–877 (2022).
pubmed: 35976622 pmcid: 9386598 doi: 10.1001/jamasurg.2022.3544
Lee, J. et al. Open and laparoscopic adrenalectomy: analysis of the National Surgical Quality Improvement Program. J. Am. Coll. Surg. 206, 953–959 (2008).
pubmed: 18471733 doi: 10.1016/j.jamcollsurg.2008.01.018
Li, J., Wang, Y., Chang, X. & Han, Z. Laparoscopic adrenalectomy (LA) vs open adrenalectomy (OA) for pheochromocytoma (PHEO): a systematic review and meta-analysis. Eur. J. Surg. Oncol. 46, 991–998 (2020).
pubmed: 32102743 doi: 10.1016/j.ejso.2020.02.009
Zelinka, T. et al. Metastatic pheochromocytoma: does the size and age matter? Eur. J. Clin. Invest. 41, 1121–1128 (2011).
pubmed: 21692797 pmcid: 3170415 doi: 10.1111/j.1365-2362.2011.02518.x
Dickson, P. V. et al. Posterior retroperitoneoscopic adrenalectomy is a safe and effective alternative to transabdominal laparoscopic adrenalectomy for pheochromocytoma. Surgery 150, 452–458 (2011).
pubmed: 21878230 doi: 10.1016/j.surg.2011.07.004
Hu, H. et al. En bloc resection with major blood vessel reconstruction for locally invasive retroperitoneal paragangliomas: a 15-year experience with literature review. World J. Surg. 41, 997–1004 (2017).
pubmed: 27896404 doi: 10.1007/s00268-016-3846-x
Abadin, S. S. et al. Impact of surgical resection for subdiaphragmatic paragangliomas. World J. Surg. 38, 733–741 (2014).
pubmed: 24390286 doi: 10.1007/s00268-013-2443-5
Cui, Y. et al. Local-regional recurrence of pheochromocytoma/paraganglioma: characteristics, risk factors and outcomes. Front. Endocrinol. 12, 762548 (2021).
doi: 10.3389/fendo.2021.762548
Li, M. L., Fitzgerald, P. A., Price, D. C. & Norton, J. A. Iatrogenic pheochromocytomatosis: a previously unreported result of laparoscopic adrenalectomy. Surgery 130, 1072–1077 (2001).
pubmed: 11742341 doi: 10.1067/msy.2001.118373
Ricketts, C. J. et al. Tumor risks and genotype-phenotype-proteotype analysis in 358 patients with germline mutations in SDHB and SDHD. Hum. Mutat. 31, 41–51 (2010).
pubmed: 19802898 doi: 10.1002/humu.21136
Hamidi, O. et al. Malignant pheochromocytoma and paraganglioma: 272 patients over 55 years. J. Clin. Endocrinol. Metab. 102, 3296–3305 (2017).
pubmed: 28605453 pmcid: 5587061 doi: 10.1210/jc.2017-00992
Roman-Gonzalez, A. et al. Impact of surgical resection of the primary tumor on overall survival in patients with metastatic pheochromocytoma or sympathetic paraganglioma. Ann. Surg. 268, 172–178 (2018).
pubmed: 28257320 doi: 10.1097/SLA.0000000000002195
Fishbein, L. et al. The North American Neuroendocrine Tumor Society consensus guidelines for surveillance and management of metastatic and/or unresectable pheochromocytoma and paraganglioma. Pancreas 50, 469–493 (2021).
pubmed: 33939658 doi: 10.1097/MPA.0000000000001792
Livingstone, M. et al. Hemodynamic stability during pheochromocytoma resection: lessons learned over the last two decades. Ann. Surg. Oncol. 22, 4175–4180 (2015).
pubmed: 25822781 doi: 10.1245/s10434-015-4519-y
Berends, A. M. A., Kerstens, M. N., Lenders, J. W. M. & Timmers, H. Approach to the patient: perioperative management of the patient with pheochromocytoma or sympathetic paraganglioma. J. Clin. Endocrinol. Metab. 105, dgaa441 (2020).
pubmed: 32726444 doi: 10.1210/clinem/dgaa441
Taieb, D. et al. Clinical consensus guideline on the management of phaeochromocytoma and paraganglioma in patients harbouring germline SDHD pathogenic variants. Lancet Diabetes Endocrinol. 11, 345–361 (2023).
pubmed: 37011647 doi: 10.1016/S2213-8587(23)00038-4
Groeben, H. et al. International multicentre review of perioperative management and outcome for catecholamine-producing tumours. Br. J. Surg. 107, e170–e178 (2020).
pubmed: 31903598 doi: 10.1002/bjs.11378
Buisset, C. et al. Pheochromocytoma surgery without systematic preoperative pharmacological preparation: insights from a referral tertiary center experience. Surg. Endosc. 35, 728–735 (2021).
pubmed: 32072283 doi: 10.1007/s00464-020-07439-1
Shao, Y. et al. Preoperative alpha blockade for normotensive pheochromocytoma: is it necessary? J. Hypertens. 29, 2429–2432 (2011).
pubmed: 22025238 doi: 10.1097/HJH.0b013e32834d24d9
Brunaud, L. et al. Both preoperative alpha and calcium channel blockade impact intraoperative hemodynamic stability similarly in the management of pheochromocytoma. Surgery 156, 1410–1417 (2014).
pubmed: 25456922 doi: 10.1016/j.surg.2014.08.022
Ulchaker, J. C., Goldfarb, D. A., Bravo, E. L. & Novick, A. C. Successful outcomes in pheochromocytoma surgery in the modern era. J. Urol. 161, 764–767 (1999).
pubmed: 10022680 doi: 10.1016/S0022-5347(01)61762-2
Groeben, H. et al. Perioperative Perioperative alpha-receptor blockade in phaeochromocytoma surgery: an observational case series. Br. J. Anaesth. 118, 182–189 (2017).-receptor blockade in phaeochromocytoma surgery: an observational case series. Br. J. Anaesth. 118, 182–189 (2017).
pubmed: 28100521 doi: 10.1093/bja/aew392
Schimmack, S. et al. Meta-analysis of α-blockade versus no blockade before adrenalectomy for phaeochromocytoma. Br. J. Surg. 107, e102–e108 (2020).
pubmed: 31903584 doi: 10.1002/bjs.11348
Buitenwerf, E. et al. Efficacy of α-blockers on hemodynamic control during pheochromocytoma resection: a randomized controlled trial. J. Clin. Endocrinol. Metab. 105, 2381–2391 (2020).
pubmed: 31714582 doi: 10.1210/clinem/dgz188
Fassnacht, M. et al. Adrenocortical carcinomas and malignant phaeochromocytomas: ESMO-EURACAN Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 31, 1476–1490 (2020).
pubmed: 32861807 doi: 10.1016/j.annonc.2020.08.2099
Neumann, H. P. et al. Distinct clinical features of paraganglioma syndromes associated with SDHB and SDHD gene mutations. JAMA 292, 943–951 (2004).
pubmed: 15328326 doi: 10.1001/jama.292.8.943
Lloyd, S., Obholzer, R. & Tysome, J.; BSBS Consensus Group. British Skull Base Society clinical consensus document on management of head and neck paragangliomas. Otolaryngol. Head Neck Surg. 163, 400–409 (2020).
pubmed: 32340547 doi: 10.1177/0194599820915490
McCrary, H. C. et al. Characterization of malignant head and neck paragangliomas at a single institution across multiple decades. JAMA Otolaryngol. Head Neck Surg. 145, 641–646 (2019).
pubmed: 31194233 pmcid: 6567840 doi: 10.1001/jamaoto.2019.1110
Richter, S. et al. Head/neck paragangliomas: focus on tumor location, mutational status and plasma methoxytyramine. Endocr. Relat. Cancer 29, 213–224 (2022).
pubmed: 35171114 pmcid: 8942340 doi: 10.1530/ERC-21-0359
Timmers, H. J., Gimenez-Roqueplo, A. P., Mannelli, M. & Pacak, K. Clinical aspects of SDHx-related pheochromocytoma and paraganglioma. Endocr. Relat. Cancer 16, 391–400 (2009).
pubmed: 19190077 pmcid: 4711350 doi: 10.1677/ERC-08-0284
Rijken, J. A. et al. Nationwide study of patients with head and neck paragangliomas carrying SDHB germline mutations. BJS Open 2, 62–69 (2018).
pubmed: 29951630 pmcid: 5952381 doi: 10.1002/bjs5.39
Wanna, G. B. et al. Subtotal resection for management of large jugular paragangliomas with functional lower cranial nerves. Otolaryngol. Head Neck Surg. 151, 991–995 (2014).
pubmed: 25261283 doi: 10.1177/0194599814552060
Manzoor, N. F. et al. Contemporary management of jugular paragangliomas with neural preservation. Otolaryngol. Head Neck Surg. 164, 391–398 (2021).
pubmed: 32660391 doi: 10.1177/0194599820938660
Sethi, R. V., Sethi, R. K., Herr, M. W. & Deschler, D. G. Malignant head and neck paragangliomas: treatment efficacy and prognostic indicators. Am. J. Otolaryngol. 34, 431–438 (2013).
pubmed: 23642313 doi: 10.1016/j.amjoto.2013.03.010
Moskovic, D. J. et al. Malignant head and neck paragangliomas: is there an optimal treatment strategy? Head Neck Oncol. 2, 23 (2010).
pubmed: 20863367 pmcid: 2956716 doi: 10.1186/1758-3284-2-23
Moore, M. G., Netterville, J. L., Mendenhall, W. M., Isaacson, B. & Nussenbaum, B. Head and neck paragangliomas: an update on evaluation and management. Otolaryngol. Head Neck Surg. 154, 597–605 (2016).
pubmed: 26861230 doi: 10.1177/0194599815627667
Ivan, M. E. et al. A meta-analysis of tumor control rates and treatment-related morbidity for patients with glomus jugulare tumors. J. Neurosurg. 114, 1299–1305 (2011).
pubmed: 21029039 doi: 10.3171/2010.9.JNS10699
Gaynor, B. G., Elhammady, M. S., Jethanamest, D., Angeli, S. I. & Aziz-Sultan, M. A. Incidence of cranial nerve palsy after preoperative embolization of glomus jugulare tumors using Onyx. J. Neurosurg. 120, 377–381 (2014).
pubmed: 24313612 doi: 10.3171/2013.10.JNS13354
Linskey, M. E. et al. Stroke risk after abrupt internal carotid artery sacrifice: accuracy of preoperative assessment with balloon test occlusion and stable xenon-enhanced CT. AJNR Am. J. Neuroradiol. 15, 829–843 (1994).
pubmed: 8059649 pmcid: 8332190
Tarr, R. W. et al. Complications of preoperative balloon test occlusion of the internal carotid arteries: experience in 300 cases. Skull Base Surg. 1, 240–244 (1991).
pubmed: 17170842 pmcid: 1656333 doi: 10.1055/s-2008-1057104
Mathis, J. M. et al. Temporary balloon test occlusion of the internal carotid artery: experience in 500 cases. AJNR Am. J. Neuroradiol. 16, 749–754 (1995).
pubmed: 7611033 pmcid: 8332245
Suarez, C. et al. Carotid body paragangliomas: a systematic study on management with surgery and radiotherapy. Eur. Arch. Otorhinolaryngol. 271, 23–34 (2014).
pubmed: 23420148 doi: 10.1007/s00405-013-2384-5
Suarez, C. et al. Jugular and vagal paragangliomas: systematic study of management with surgery and radiotherapy. Head Neck 35, 1195–1204 (2013).
pubmed: 22422597 doi: 10.1002/hed.22976
Makis, W., McCann, K., McEwan, A. J. & Sawyer, M. B. Combined treatment with 131I-MIBG and sunitinib induces remission in a patient with metastatic paraganglioma due to hereditary paraganglioma-pheochromocytoma syndrome from an SDHB mutation. Clin. Nucl. Med. 41, 204–206 (2016).
pubmed: 26359568 doi: 10.1097/RLU.0000000000000973
Ibuki, N. et al. A pheochromocytoma of urinary bladder treated with neoadjuvant chemotherapy [Japanese]. Hinyokika Kiyo 55, 765–768 (2009).
pubmed: 20048562
Visani, J. et al. Surgical treatment of metastatic pheochromocytomas of the spine: a systematic review. J. Integr. Neurosci. 20, 499–507 (2021).
pubmed: 34258952 doi: 10.31083/j.jin2002053
Bizzarri, N. et al. Peritoneal carcinomatosis from ovarian paraganglioma: report of a rare case and systematic review of the literature. J. Obstet. Gynaecol. Res. 44, 1682–1692 (2018).
pubmed: 29978527 doi: 10.1111/jog.13713
Amar, L. et al. MANAGEMENT OF ENDOCRINE DISEASE: recurrence or new tumors after complete resection of pheochromocytomas and paragangliomas: a systematic review and meta-analysis. Eur. J. Endocrinol. 175, R135–R145 (2016).
pubmed: 27080352 doi: 10.1530/EJE-16-0189
Holscher, I., van den Berg, T. J., Dreijerink, K. M. A., Engelsman, A. F. & Nieveen van Dijkum, E. J. M. Recurrence rate of sporadic pheochromocytomas after curative adrenalectomy: a systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 106, 588–597 (2021).
pubmed: 33125073 doi: 10.1210/clinem/dgaa794
Wachtel, H. et al. Predicting metastatic potential in pheochromocytoma and paraganglioma: a comparison of PASS and GAPP scoring systems. J. Clin. Endocrinol. Metab. 105, 4661–4670 (2020).
doi: 10.1210/clinem/dgaa608
Eisenhofer, G. et al. Biochemical and clinical manifestations of dopamine-producing paragangliomas: utility of plasma methoxytyramine. J. Clin. Endocrinol. Metab. 90, 2068–2075 (2005).
pubmed: 15644397 doi: 10.1210/jc.2004-2025
Pamporaki, C. et al. Determinants of disease-specific survival in patients with and without metastatic pheochromocytoma and paraganglioma. Eur. J. Cancer 169, 32–41 (2022).
pubmed: 35500459 doi: 10.1016/j.ejca.2022.03.032
Fishbein, L. et al. External beam radiation therapy (EBRT) for patients with malignant pheochromocytoma and non-head and -neck paraganglioma: combination with
pubmed: 22566196 pmcid: 4357844 doi: 10.1055/s-0032-1308992
Mesko, S. et al. Spine stereotactic radiosurgery for metastatic pheochromocytoma. Cureus 11, e4742 (2019).
pubmed: 31355101 pmcid: 6649891
Ayala-Ramirez, M. et al. Bone metastases and skeletal-related events in patients with malignant pheochromocytoma and sympathetic paraganglioma. J. Clin. Endocrinol. Metab. 98, 1492–1497 (2013).
pubmed: 23436918 pmcid: 5393459 doi: 10.1210/jc.2012-4231
Gravel, G. et al. Prevention of serious skeletal-related events by interventional radiology techniques in patients with malignant paraganglioma and pheochromocytoma. Endocrine 59, 547–554 (2018).
pubmed: 29305799 doi: 10.1007/s12020-017-1515-y
Pacak, K. et al. Radiofrequency ablation: a novel approach for treatment of metastatic pheochromocytoma. J. Natl Cancer Inst. 93, 648–649 (2001).
pubmed: 11309443 doi: 10.1093/jnci/93.8.648
Venkatesan, A. M. et al. Radiofrequency ablation of metastatic pheochromocytoma. J. Vasc. Interv. Radiol. 20, 1483–1490 (2009).
pubmed: 19875067 pmcid: 3608423 doi: 10.1016/j.jvir.2009.07.031
Zhang, W. et al. Computed tomography-guided cryoablation for adrenal pheochromocytoma: safety and clinical effectiveness. Surg. Laparosc. Endosc. Percutan. Tech. 29, 409–412 (2019).
pubmed: 31107857 doi: 10.1097/SLE.0000000000000677
Kohlenberg, J. et al. Efficacy and safety of ablative therapy in the treatment of patients with metastatic pheochromocytoma and paraganglioma. Cancers 11, 195 (2019).
pubmed: 30736463 pmcid: 6407137 doi: 10.3390/cancers11020195
Deljou, A. et al. Hemodynamic instability during percutaneous ablation of extra-adrenal metastases of pheochromocytoma and paragangliomas: a case series. BMC Anesthesiol. 18, 158 (2018).
pubmed: 30400849 pmcid: 6220566 doi: 10.1186/s12871-018-0626-1
Hidaka, S. et al. Malignant pheochromocytoma with liver metastasis treated by transcatheter arterial chemo-embolization (TACE). Intern. Med. 49, 645–651 (2010).
pubmed: 20371953 doi: 10.2169/internalmedicine.49.3061
Hescot, S. et al. One-year progression-free survival of therapy-naive patients with malignant pheochromocytoma and paraganglioma. J. Clin. Endocrinol. Metab. 98, 4006–4012 (2013).
pubmed: 23884775 doi: 10.1210/jc.2013-1907
Hescot, S. et al. Prognosis of malignant pheochromocytoma and paraganglioma (MAPP-Prono study): an ENS@T retrospective study. J. Clin. Endocrinol. Metab. 104, 2367–2374 (2019).
pubmed: 30715419 doi: 10.1210/jc.2018-01968
Dhir, M. et al. Clinical predictors of malignancy in patients with pheochromocytoma and paraganglioma. Ann. Surg. Oncol. 24, 3624–3630 (2017).
pubmed: 28884434 doi: 10.1245/s10434-017-6074-1
Jochmanova, I. et al. Clinical characteristics and outcomes of SDHB-related pheochromocytoma and paraganglioma in children and adolescents. J. Cancer Res. Clin. Oncol. 146, 1051–1063 (2020).
pubmed: 32062700 pmcid: 7388579 doi: 10.1007/s00432-020-03138-5
Nolting, S. et al. Current management of pheochromocytoma/paraganglioma: a guide for the practicing clinician in the era of precision medicine. Cancers 11, 1505 (2019).
pubmed: 31597347 pmcid: 6827093 doi: 10.3390/cancers11101505
Zheng, L. et al. Hypertensive crisis during microwave ablation of adrenal neoplasms: a retrospective analysis of predictive factors. J. Vasc. Interv. Radiol. 30, 1343–1350 (2019).
pubmed: 31155498 doi: 10.1016/j.jvir.2019.01.016
Eisenhofer, G. et al. Adverse drug reactions in patients with phaeochromocytoma: incidence, prevention and management. Drug Saf. 30, 1031–1062 (2007).
pubmed: 17973541 doi: 10.2165/00002018-200730110-00004
Pacak, K. Preoperative management of the pheochromocytoma patient. J. Clin. Endocrinol. Metab. 92, 4069–4079 (2007).
pubmed: 17989126 doi: 10.1210/jc.2007-1720
Nazari, M. A., Rosenblum, J. S., Haigney, M. C., Rosing, D. R. & Pacak, K. Pathophysiology and acute management of tachyarrhythmias in pheochromocytoma: JACC review topic of the week. J. Am. Coll. Cardiol. 76, 451–464 (2020).
pubmed: 32703516 pmcid: 7454044 doi: 10.1016/j.jacc.2020.04.080
Talvacchio, S., Nazari, M. A. & Pacak, K. Supportive management of patients with pheochromocytoma/paraganglioma undergoing noninvasive treatment. Curr. Opin. Endocrinol. Diabetes Obes. 29, 294–301 (2022).
pubmed: 35621181 pmcid: 9205066 doi: 10.1097/MED.0000000000000724
Huang, H. et al. Treatment of malignant pheochromocytoma/paraganglioma with cyclophosphamide, vincristine, and dacarbazine: recommendation from a 22-year follow-up of 18 patients. Cancer 113, 2020–2028 (2008).
pubmed: 18780317 doi: 10.1002/cncr.23812
Averbuch, S. D. et al. Malignant pheochromocytoma: effective treatment with a combination of cyclophosphamide, vincristine, and dacarbazine. Ann. Intern. Med. 109, 267–273 (1988).
pubmed: 3395037 doi: 10.7326/0003-4819-109-4-267
Niemeijer, N. D., Alblas, G., van Hulsteijn, L. T., Dekkers, O. M. & Corssmit, E. P. Chemotherapy with cyclophosphamide, vincristine and dacarbazine for malignant paraganglioma and pheochromocytoma: systematic review and meta-analysis. Clin. Endocrinol. 81, 642–651 (2014).
doi: 10.1111/cen.12542
Asai, S., Katabami, T., Tsuiki, M., Tanaka, Y. & Naruse, M. Controlling tumor progression with cyclophosphamide, vincristine, and dacarbazine treatment improves survival in patients with metastatic and unresectable malignant pheochromocytomas/paragangliomas. Horm. Cancer 8, 108–118 (2017).
pubmed: 28108930 pmcid: 10355862 doi: 10.1007/s12672-017-0284-7
Deutschbein, T. et al. Treatment of malignant phaeochromocytoma with a combination of cyclophosphamide, vincristine and dacarbazine: own experience and overview of the contemporary literature. Clin. Endocrinol. 82, 84–90 (2015).
doi: 10.1111/cen.12590
Tanabe, A. et al. Combination chemotherapy with cyclophosphamide, vincristine, and dacarbazine in patients with malignant pheochromocytoma and paraganglioma. Horm. Cancer 4, 103–110 (2013).
pubmed: 23361939 pmcid: 10358011 doi: 10.1007/s12672-013-0133-2
Jawed, I. et al. Continued tumor reduction of metastatic pheochromocytoma/paraganglioma harboring succinate dehydrogenase subunit b mutations with cyclical chemotherapy. Cell Mol. Neurobiol. 38, 1099–1106 (2018).
pubmed: 29623478 pmcid: 5976545 doi: 10.1007/s10571-018-0579-4
Fishbein, L. et al. SDHB mutation carriers with malignant pheochromocytoma respond better to CVD. Endocr. Relat. Cancer 24, L51–L55 (2017).
pubmed: 28566531 doi: 10.1530/ERC-17-0086
Pacheco, S. T. et al. Metastatic pheochromocytoma and paraganglioma: a retrospective multicentre analysis on prognostic and predictive factors to chemotherapy. Ecancermedicalscience 17, 1523 (2023).
pubmed: 37113718 pmcid: 10129398 doi: 10.3332/ecancer.2023.1523
Fischer, A. et al. Responses to systemic therapy in metastatic pheochromocytoma/paraganglioma - a retrospective multi-center cohort study. Eur. J. Endocrinol. https://doi.org/10.1093/ejendo/lvad146 (2023).
doi: 10.1093/ejendo/lvad146 pubmed: 37949483
Shah, M. H. et al. Neuroendocrine and adrenal tumors, version 2.2021, NCCN clinical practice guidelines in oncology. J. Natl Compr. Canc. Netw. 19, 839–868 (2021).
pubmed: 34340212 doi: 10.6004/jnccn.2021.0032
Benn, D. E. et al. Clinical presentation and penetrance of pheochromocytoma/paraganglioma syndromes. J. Clin. Endocrinol. Metab. 91, 827–836 (2006).
pubmed: 16317055 doi: 10.1210/jc.2005-1862
Petrak, O. et al. Blood pressure profile, catecholamine phenotype, and target organ damage in pheochromocytoma/paraganglioma. J. Clin. Endocrinol. Metab. 104, 5170–5180 (2019).
pubmed: 31009053 doi: 10.1210/jc.2018-02644
Gonias, S. et al. Phase II study of high-dose [
pubmed: 19636009 pmcid: 2734428 doi: 10.1200/JCO.2008.21.3496
Pryma, D. A. et al. Efficacy and safety of high-specific-activity
pubmed: 30291194 pmcid: 6495236 doi: 10.2967/jnumed.118.217463
Makis, W., McCann, K. & McEwan, A. J. The challenges of treating paraganglioma patients with
pubmed: 26279696 pmcid: 4532685 doi: 10.1007/s13139-015-0332-6
Zandee, W. T. et al. Treatment of inoperable or metastatic paragangliomas and pheochromocytomas with peptide receptor radionuclide therapy using
pubmed: 31067510 doi: 10.1530/EJE-18-0901
van Hulsteijn, L. T., Niemeijer, N. D., Dekkers, O. M. & Corssmit, E. P.
doi: 10.1111/cen.12341
Satapathy, S., Mittal, B. R. & Bhansali, A. Peptide receptor radionuclide therapy in the management of advanced pheochromocytoma and paraganglioma: a systematic review and meta-analysis. Clin. Endocrinol. 91, 718–727 (2019).
doi: 10.1111/cen.14106
Nastos, K. et al. Peptide receptor radionuclide treatment and
pubmed: 28166370 doi: 10.1002/jso.24553
Carrasquillo, J. A. et al. Systemic radiopharmaceutical therapy of pheochromocytoma and paraganglioma. J. Nucl. Med. 62, 1192–1199 (2021).
pubmed: 34475242 pmcid: 8882896 doi: 10.2967/jnumed.120.259697
Fonte, J. S. et al. False-negative
pubmed: 22167067 pmcid: 3420013 doi: 10.1530/ERC-11-0243
Timmers, H. J. et al. Superiority of fluorodeoxyglucose positron emission tomography to other functional imaging techniques in the evaluation of metastatic SDHB-associated pheochromocytoma and paraganglioma. J. Clin. Oncol. 25, 2262–2269 (2007).
pubmed: 17538171 doi: 10.1200/JCO.2006.09.6297
Timmers, H. J. et al. Comparison of
pubmed: 19864450 pmcid: 2795662 doi: 10.1210/jc.2009-1248
Petenuci, J. et al. SDHB large deletions are associated with absence of MIBG uptake in metastatic lesions of malignant paragangliomas. Endocrine 72, 586–590 (2021).
pubmed: 33420946 doi: 10.1007/s12020-020-02594-w
Lynn, M. D. et al. Portrayal of pheochromocytoma and normal human adrenal medulla by m-[
pubmed: 6544815
Donato, S., Simoes, H., Pinto, A. T., B, M. C. & Leite, V. SDHx-related pheochromocytoma/paraganglioma — genetic, clinical, and treatment outcomes in a series of 30 patients from a single center. Endocrine 65, 408–415 (2019).
pubmed: 31104306 doi: 10.1007/s12020-019-01953-6
Carrasquillo, J. A., Pandit-Taskar, N. & Chen, C. C. I-131 metaiodobenzylguanidine therapy of pheochromocytoma and paraganglioma. Semin. Nucl. Med. 46, 203–214 (2016).
pubmed: 27067501 doi: 10.1053/j.semnuclmed.2016.01.011
Amar, L. et al. Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. J. Clin. Endocrinol. Metab. 92, 3822–3828 (2007).
pubmed: 17652212 doi: 10.1210/jc.2007-0709
Ayala-Ramirez, M. et al. Clinical risk factors for malignancy and overall survival in patients with pheochromocytomas and sympathetic paragangliomas: primary tumor size and primary tumor location as prognostic indicators. J. Clin. Endocrinol. Metab. 96, 717–725 (2011).
pubmed: 21190975 doi: 10.1210/jc.2010-1946
Noto, R. B. et al. Phase 1 study of high-specific-activity I-131 MIBG for metastatic and/or recurrent pheochromocytoma or paraganglioma. J. Clin. Endocrinol. Metab. 103, 213–220 (2018).
pubmed: 29099942 doi: 10.1210/jc.2017-02030
Safford, S. D. et al. Iodine -131 metaiodobenzylguanidine is an effective treatment for malignant pheochromocytoma and paraganglioma. Surgery 134, 956–962 (2003).
pubmed: 14668728 doi: 10.1016/S0039-6060(03)00426-4
Thorpe, M. P. et al. Long-term outcomes of 125 patients with metastatic pheochromocytoma or paraganglioma treated with 131-I MIBG. J. Clin. Endocrinol. Metab. 105, e494–e501 (2020).
pubmed: 31614368 doi: 10.1210/clinem/dgz074
Elston, M. S. et al. Increased SSTR2A and SSTR3 expression in succinate dehydrogenase-deficient pheochromocytomas and paragangliomas. Hum. Pathol. 46, 390–396 (2015).
pubmed: 25554089 doi: 10.1016/j.humpath.2014.11.012
Kaemmerer, D. et al. Evaluation of somatostatin, CXCR4 chemokine and endothelin A receptor expression in a large set of paragangliomas. Oncotarget 8, 89958–89969 (2017).
pubmed: 29163802 pmcid: 5685723 doi: 10.18632/oncotarget.21194
Fischer, A. et al. Metastatic pheochromocytoma and paraganglioma: somatostatin receptor 2 expression, genetics and therapeutic responses. J. Clin. Endocrinol. Metab. 108, 2676–2685 (2023).
pubmed: 36946182 pmcid: 10505550 doi: 10.1210/clinem/dgad166
Roll, W. et al. Somatostatin receptor-targeted radioligand therapy in head and neck paraganglioma. World Neurosurg. 143, e391–e399 (2020).
pubmed: 32745642 doi: 10.1016/j.wneu.2020.07.165
Tsang, E. S., Funk, G., Leung, J., Kalish, G. & Kennecke, H. F. Supportive management of patients with advanced pheochromocytomas and paragangliomas receiving PRRT. Curr. Oncol. 28, 2823–2829 (2021).
pubmed: 34436013 pmcid: 8395467 doi: 10.3390/curroncol28040247
Pinato, D. J. et al. Peptide receptor radionuclide therapy for metastatic paragangliomas. Med. Oncol. 33, 47 (2016).
pubmed: 27059363 doi: 10.1007/s12032-016-0737-9
Kolasinska-Cwikla, A. et al. A clinical efficacy of PRRT in patients with advanced, nonresectable, paraganglioma-pheochromocytoma, related to SDHx gene mutation. J. Clin. Med. 8, 952 (2019).
pubmed: 31262070 pmcid: 6678858 doi: 10.3390/jcm8070952
Vyakaranam, A. R. et al. Favorable outcome in patients with pheochromocytoma and paraganglioma treated with
pubmed: 31261748 pmcid: 6678507 doi: 10.3390/cancers11070909
Hadoux, J. et al. SDHB mutations are associated with response to temozolomide in patients with metastatic pheochromocytoma or paraganglioma. Int. J. Cancer 135, 2711–2720 (2014).
pubmed: 24752622 doi: 10.1002/ijc.28913
Eisenhauer, E. A. et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer 45, 228–247 (2009).
pubmed: 19097774 doi: 10.1016/j.ejca.2008.10.026
O, J. H., Lodge, M. A. & Wahl, R. L. Practical PERCIST: a simplified guide to PET response criteria in solid tumors 1.0. Radiology 280, 576–584 (2016).
pubmed: 26909647 doi: 10.1148/radiol.2016142043
Hegi, M. E. et al. Correlation of O6-methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity. J. Clin. Oncol. 26, 4189–4199 (2008).
pubmed: 18757334 doi: 10.1200/JCO.2007.11.5964
Zhou, Y., Cui, Y., Zhang, D. & Tong, A. Efficacy and safety of tyrosine kinase inhibitors in patients with metastatic pheochromocytomas/paragangliomas. J. Clin. Endocrinol. Metab. 108, 755–766 (2023).
pubmed: 36383456 doi: 10.1210/clinem/dgac657
O’Kane, G. M. et al. A phase 2 trial of sunitinib in patients with progressive paraganglioma or pheochromocytoma: the SNIPP trial. Br. J. Cancer 120, 1113–1119 (2019).
pubmed: 31105270 pmcid: 6738062 doi: 10.1038/s41416-019-0474-x
Ayala-Ramirez, M. et al. Treatment with sunitinib for patients with progressive metastatic pheochromocytomas and sympathetic paragangliomas. J. Clin. Endocrinol. Metab. 97, 4040–4050 (2012).
pubmed: 22965939 pmcid: 3683800 doi: 10.1210/jc.2012-2356
Baudin, E. et al. 567O_PR — First international randomized study in malignant progressive pheochromocytoma and paragangliomas (FIRSTMAPPP): an academic double-blind trial investigating sunitinib. Ann. Oncol. 32, S621–S625 (2021).
doi: 10.1016/j.annonc.2021.08.702
Jimenez C, P. M., Busaidy N, Habra MA, Waguespack S, Jessop A. A phase 2 study to evaluate the effects of cabozantinib in patients with unresectable metastatic pheochromocytomas and paragangliomas. International Symposium on Pheochromocytoma and Paraganglioma (Sydney, Australia, 2017).
Naing, A. et al. Phase 2 study of pembrolizumab in patients with advanced rare cancers. J. Immunother. Cancer 8, e000347 (2020).
pubmed: 32188704 pmcid: 7078933 doi: 10.1136/jitc-2019-000347
Jimenez, C. et al. Phase II clinical trial of pembrolizumab in patients with progressive metastatic pheochromocytomas and paragangliomas. Cancers 12, 2307 (2020).
pubmed: 32824391 pmcid: 7465458 doi: 10.3390/cancers12082307
Caplin, M. E. et al. Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N. Engl. J. Med. 371, 224–233 (2014).
pubmed: 25014687 doi: 10.1056/NEJMoa1316158
Pavel, M. et al. Gastroenteropancreatic neuroendocrine neoplasms: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 31, 844–860 (2020).
pubmed: 32272208 doi: 10.1016/j.annonc.2020.03.304
Rinke, A. et al. Placebo-controlled, double-blind, prospective, randomized study on the effect of octreotide LAR in the control of tumor growth in patients with metastatic neuroendocrine midgut tumors: a report from the PROMID Study Group. J. Clin. Oncol. 27, 4656–4663 (2009).
pubmed: 19704057 doi: 10.1200/JCO.2009.22.8510
Greenberg, S. E. et al. Tumor detection rates in screening of individuals with SDHx-related hereditary paraganglioma-pheochromocytoma syndrome. Genet. Med. 22, 2101–2107 (2020).
pubmed: 32741965 pmcid: 7710583 doi: 10.1038/s41436-020-0921-3
Hes, F. J. et al. Low penetrance of a SDHB mutation in a large Dutch paraganglioma family. BMC Med. Genet. 11, 92 (2010).
pubmed: 20540712 pmcid: 2891715 doi: 10.1186/1471-2350-11-92
Papathomas, T. G. et al. SDHB/SDHA immunohistochemistry in pheochromocytomas and paragangliomas: a multicenter interobserver variation analysis using virtual microscopy: a Multinational Study of the European Network for the Study of Adrenal Tumors (ENS@T). Mod. Pathol. 28, 807–821 (2015).
pubmed: 25720320 doi: 10.1038/modpathol.2015.41
Pasini, B. & Stratakis, C. A. SDH mutations in tumorigenesis and inherited endocrine tumours: lesson from the phaeochromocytoma-paraganglioma syndromes. J. Intern. Med. 266, 19–42 (2009).
pubmed: 19522823 doi: 10.1111/j.1365-2796.2009.02111.x
Rijken, J. A. et al. Low penetrance of paraganglioma and pheochromocytoma in an extended kindred with a germline SDHB exon 3 deletion. Clin. Genet. 89, 128–132 (2016).
pubmed: 25827221 doi: 10.1111/cge.12591
Schiavi, F. et al. Are we overestimating the penetrance of mutations in SDHB? Hum. Mutat. 31, 761–762 (2010).
pubmed: 20513144 doi: 10.1002/humu.21269
Solis, D. C. et al. Penetrance and clinical consequences of a gross SDHB deletion in a large family. Clin. Genet. 75, 354–363 (2009).
pubmed: 19389109 pmcid: 4718153 doi: 10.1111/j.1399-0004.2009.01157.x
Timmers, H. J. et al. Clinical presentations, biochemical phenotypes, and genotype-phenotype correlations in patients with succinate dehydrogenase subunit B-associated pheochromocytomas and paragangliomas. J. Clin. Endocrinol. Metab. 92, 779–786 (2007).
pubmed: 17200167 doi: 10.1210/jc.2006-2315
van Hulsteijn, L. T., Dekkers, O. M., Hes, F. J., Smit, J. W. & Corssmit, E. P. Risk of malignant paraganglioma in SDHB-mutation and SDHD-mutation carriers: a systematic review and meta-analysis. J. Med. Genet. 49, 768–776 (2012).
pubmed: 23099648 doi: 10.1136/jmedgenet-2012-101192
Taieb, D., Jha, A., Treglia, G. & Pacak, K. Molecular imaging and radionuclide therapy of pheochromocytoma and paraganglioma in the era of genomic characterization of disease subgroups. Endocr. Relat. Cancer 26, R627–R652 (2019).
pubmed: 31561209 pmcid: 7002202 doi: 10.1530/ERC-19-0165

Auteurs

David Taïeb (D)

Department of Nuclear Medicine, Aix-Marseille University, La Timone University Hospital, Marseille, France.

Svenja Nölting (S)

Department of Endocrinology, Diabetology and Clinical Nutrition, University Hospital Zurich and University of Zurich, Zurich, Switzerland.
Department of Medicine IV, University Hospital, Ludwig-Maximilians-University Munich, Munich, Germany.

Nancy D Perrier (ND)

Department of Surgical Oncology, MD Anderson Cancer Center, Houston, TX, USA.

Martin Fassnacht (M)

Department of Medicine, Division of Endocrinology and Diabetes, University Hospital, University of Würzburg, Würzburg, Germany.
ORCID: 0000-0001-6170-6398

Jorge A Carrasquillo (JA)

Molecular Imaging and Therapy Service, Radiology Department, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
ORCID: 0000-0002-8513-5734

Ashley B Grossman (AB)

Green Templeton College, University of Oxford, Oxford, UK.
NET Unit, Royal Free Hospital, London, UK.
ORCID: 0000-0003-1176-6186

Roderick Clifton-Bligh (R)

Department of Endocrinology, Royal North Shore Hospital and Cancer Genetics Laboratory, Kolling Institute, University of Sydney, Sydney, New South Wales, Australia.
ORCID: 0000-0002-1545-0368

George B Wanna (GB)

Department of Otolaryngology-Head and Neck Surgery, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Zachary G Schwam (ZG)

Department of Otolaryngology-Head and Neck Surgery, Icahn School of Medicine at Mount Sinai, New York, NY, USA.

Laurence Amar (L)

Université Paris Cité, Inserm, PARCC, Equipe Labellisée par la Ligue contre le Cancer, Paris, France.
Hypertension Unit, Hôpital Européen Georges Pompidou, Assistance Publique - Hôpitaux de Paris, Paris, France.
ORCID: 0000-0003-3942-4276

Isabelle Bourdeau (I)

Division of Endocrinology, Department of Medicine and Research Center, Centre hospitalier de l'Université de Montréal (CHUM), Montréal, Québec, Canada.

Ruth T Casey (RT)

Department of Medical Genetics, University of Cambridge, Cambridge Biomedical Campus, Cambridge, UK.

Joakim Crona (J)

Department of Medical Sciences, Uppsala University, Uppsala, Sweden.
ORCID: 0000-0003-0677-4894

Cheri L Deal (CL)

Research Center, CHU Sainte-Justine and Dept. of Paediatrics, University of Montreal, Montreal, Québec, Canada.
ORCID: 0000-0001-6434-2745

Jaydira Del Rivero (J)

Developmental Therapeutics Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Quan-Yang Duh (QY)

Department of Surgery, UCSF-Mount Zion, San Francisco, CA, USA.

Graeme Eisenhofer (G)

Institute of Clinical Chemistry and Laboratory Medicine, University Hospital Carl Gustav Carus at the TU Dresden, Dresden, Germany.

Tito Fojo (T)

Columbia University Irving Medical Center, New York City, NY, USA.
James J. Peters VA Medical Center, New York City, NY, USA.

Hans K Ghayee (HK)

Division of Endocrinology & Metabolism, Department of Medicine, University of Florida, Gainesville, FL, USA.
Malcom Randall VA Medical Center, Gainesville, FL, USA.

Anne-Paule Gimenez-Roqueplo (AP)

Université Paris Cité, Inserm, PARCC, Equipe Labellisée par la Ligue contre le Cancer, Paris, France.
Department of Oncogenetics and Cancer Genomic Medicine, AP-HP, Hôpital européen Georges Pompidou, Paris, France.
ORCID: 0000-0002-4816-670X

Antony J Gill (AJ)

University of Sydney, Sydney NSW Australia, Cancer Diagnosis and Pathology Group Kolling Institute of Medical Research, Royal North Shore Hospital, St Leonards, New South Wales, Australia.
NSW Health Pathology Department of Anatomical Pathology, Royal North Shore Hospital, St Leonards, New South Wales, Australia.

Rodney Hicks (R)

Department of Medicine, St Vincent's Hospital Medical School, Melbourne, Victoria, Australia.

Alessio Imperiale (A)

Department of Nuclear Medicine and Molecular Imaging - Institut de Cancérologie de Strasbourg Europe (ICANS), IPHC, UMR 7178, CNRS, University of Strasbourg, Strasbourg, France.

Abhishek Jha (A)

Section on Medical Neuroendocrinology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA.
ORCID: 0000-0002-1489-2471

Michiel N Kerstens (MN)

Department of Endocrinology, University Medical Center Groningen, Groningen, Netherlands.

Ronald R de Krijger (RR)

Department of Pathology, University Medical Center Utrecht, Utrecht, Netherlands.
Princess Máxima Center for paediatric oncology, Utrecht, Netherlands.

André Lacroix (A)

Division of Endocrinology, Department of Medicine, Centre de recherche du Centre hospitalier de l'Université de Montréal, Université de Montréal, Montréal, Canada.
ORCID: 0000-0003-4137-3025

Ivica Lazurova (I)

Department of Internal Medicine 1, University Hospital, P.J. Šafárik University, Košice, Slovakia.

Frank I Lin (FI)

Molecular Imaging Program, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Charlotte Lussey-Lepoutre (C)

Université Paris Cité, Inserm, PARCC, Equipe Labellisée par la Ligue contre le Cancer, Paris, France.
Sorbonne University, Department of Nuclear Medicine, Pitié-Salpêtrière, Paris, France.
ORCID: 0000-0003-2228-0106

Eamonn R Maher (ER)

Department of Medical Genetics, University of Cambridge, Cambridge Biomedical Campus, Cambridge, UK.
ORCID: 0000-0002-6226-6918

Ozgur Mete (O)

Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada.

Mitsuhide Naruse (M)

Clinical Research Institute of Endocrinology and Metabolism, National Hospital Organization Kyoto Medical Center and Endocrine Center, Kyoto, Japan.
Clinical Research Center, Ijinkai Takeda General Hospital, Kyoto, Japan.

Naris Nilubol (N)

Surgical Oncology Program, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Mercedes Robledo (M)

Hereditary Endocrine Cancer Group, Spanish National Cancer Research Center (CNIO), Madrid, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Institute of Health Carlos III (ISCIII), Madrid, Spain.
ORCID: 0000-0001-6256-5902

Frédéric Sebag (F)

Department of Endocrine Surgery, Aix-Marseille University, Conception Hospital, Marseille, France.

Nalini S Shah (NS)

Department of Endocrinology, Seth GS Medical College and KEM Hospital, Mumbai, Maharashtra, India.

Akiyo Tanabe (A)

Department of Diabetes, Endocrinology and Metabolism, National Center for Global Health and Medicine, Tokyo, Japan.
ORCID: 0000-0002-5682-4952

Geoffrey B Thompson (GB)

Division of Endocrine Surgery, Department of Surgery, Mayo Clinic, Rochester, MN, USA.

Henri J L M Timmers (HJLM)

Department of Internal Medicine, Radboud University Medical Center, Nijmegen, Netherlands.

Jiri Widimsky (J)

Third Department of Medicine, Department of Endocrinology and Metabolism of the First Faculty of Medicine, Charles University and General University Hospital, Prague, Czech Republic.

William J Young (WJ)

Division of Endocrinology, Diabetes, Metabolism, and Nutrition, Mayo Clinic, Rochester, MN, USA.

Leah Meuter (L)

Stanford University School of Medicine, Department of Physician Assistant Studies, Stanford, CA, USA.

Jacques W M Lenders (JWM)

Department of Internal Medicine, Radboud University Medical Center, Nijmegen, Netherlands.
ORCID: 0000-0002-7658-4466

Karel Pacak (K)

Section on Medical Neuroendocrinology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA. karel@mail.nih.gov.
ORCID: 0000-0002-3541-3767

Classifications MeSH