The DOI matches its Crossref record; 35 of the 35 references it cites were found in a registry or an index.
Krebs Cycle Metabolite Profiling for Identification and Stratification of Pheochromocytomas/Paragangliomas due to Succinate Dehydrogenase Deficiency
Open accessAbstract
Context: Mutations of succinate dehydrogenase A/B/C/D genes (SDHx) increase susceptibility to development of pheochromocytomas and paragangliomas (PPGLs), with particularly high rates of malignancy associated with SDHB mutations. Objective: We assessed whether altered succinate dehydrogenase product-precursor relationships, manifested by differences in tumor ratios of succinate to fumarate or other metabolites, might aid in identifying and stratifying patients with SDHx mutations. Design, Setting, and Patients: PPGL tumor specimens from 233 patients, including 45 with SDHx mutations, were provided from eight tertiary referral centers for mass spectrometric analyses of Krebs cycle metabolites. Main Outcome Measure: Diagnostic performance of the succinate:fumarate ratio for identification of pathogenic SDHx mutations. Results: SDH-deficient PPGLs were characterized by 25-fold higher succinate and 80% lower fumarate, cis-aconitate, and isocitrate tissue levels than PPGLs without SDHx mutations. Receiver-operating characteristic curves for use of ratios of succinate to fumarate or to cis-aconitate and isocitrate to identify SDHx mutations indicated areas under curves of 0.94 to 0.96; an optimal cut-off of 97.7 for the succinate:fumarate ratio provided a diagnostic sensitivity of 93% at a specificity of 97% to identify SDHX-mutated PPGLs. Succinate:fumarate ratios were higher in both SDHB-mutated and metastatic tumors than in those due to SDHD/C mutations or without metastases. Conclusions: Mass spectrometric-based measurements of ratios of succinate:fumarate and other metabolites in PPGLs offer a useful method to identify patients for testing of SDHx mutations, with additional utility to quantitatively assess functionality of mutations and metabolic factors responsible for malignant risk.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“In 2008, mutation of SDH was discovered in cancers such as paraganglioma and pheochromocytoma cells124. Later, similar observations were made in gastrointestinal tumors, neuroblastomas, renal tumors, thyroid tumors, and testicular tumors125,126.”
From Glutamine reliance in cell metabolism (2020) · cites this paper as [124]
Citations
Cites
Succinate is an inflammatory signal that induces IL-1β through HIF-1α
Tannahill, G. M., Curtis, A. M., Adamik, J., Palsson-McDermott, E. M., McGettrick, A. F., Goel, G., Frezza, C., Bernard, N. J., Kelly, B., Foley, N. H., et al. (2013) · Nature · doi:10.1038/nature11986 · Cited by 4,176
Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase
Selak, M. A., Armour, S. M., MacKenzie, E. D., Boulahbel, H., Watson, D. G., Mansfield, K. D., Pan, Y., Simon, M. C., Thompson, C. B., & Gottlieb, E. (2005) · Cancer Cell · doi:10.1016/j.ccr.2004.11.022 · Cited by 2,108
Pollard, P. J., Brière, J. J., Alam, N. A., Barwell, J., Barclay, E., Wortham, N. C., Hunt, T., Mitchell, M., Olpin, S., Moat, S. J., et al. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi227 · Cited by 865
2-hydroxyglutarate detection by magnetic resonance spectroscopy in IDH-mutated patients with gliomas
Choi, C., Ganji, S. K., DeBerardinis, R. J., Hatanpaa, K. J., Rakheja, D., Kovacs, Z., Yang, X.-L., Mashimo, T., Raisanen, J. M., Marin-Valencia, I., et al. (2012) · Nature Medicine · doi:10.1038/nm.2682 · Cited by 839
SDH mutations establish a hypermethylator phenotype in paraganglioma
Letouzé, E., Martinelli, C., Loriot, C., Burnichon, N., Abermil, N., Ottolenghi, C., Janin, M., Menara, M., Nguyen, A. T., Benit, P., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.04.018 · Cited by 776
Janeway, K. A., Kim, S. Y., Lodish, M., Nosé, V., Rustin, P., Gaal, J., Dahia, P. L. M., Liegl, B., Ball, E. R., Raygada, M., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009199108 · Cited by 628
Mutations in the SDHB gene are associated with extra-adrenal and/or malignant phaeochromocytomas.
Gimenez‐Roqueplo, A., Favier, J., Rustin, P., Rieubland, C., Crespin, M., Nau, V., Kien, P. K. V., Corvol, P. L., Plouin, P., & Jeunemaı̂tre, X. (2003) · PubMed · Cited by 542
Eisenhofer, G., Lenders, J. W. M., Siegert, G., Bornstein, S. R., Friberg, P., Milosevic, D., Mannelli, M., Linehan, W. M., Adams, K. T., Timmers, H. J. L. M., et al. (2011) · European Journal of Cancer · doi:10.1016/j.ejca.2011.07.016 · Cited by 375
Self-citationGermline SDHB Mutations and Familial Renal Cell Carcinoma
Ricketts, C. J., Woodward, E. R., Killick, P., Morris, M. R., Astuti, D., Latif, F., & Maher, E. R. (2008) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djn254 · Cited by 354
An Update on the Genetics of Paraganglioma, Pheochromocytoma, and Associated Hereditary Syndromes
Gimenez‐Roqueplo, A., Dahia, P. L. M., & Robledo, M. (2012) · Hormone and Metabolic Research · doi:10.1055/s-0031-1301302 · Cited by 289
Self-citation
Cited by
Sorted by citations
Glutamine reliance in cell metabolism
Yoo, H. C., Yu, Y. C., Sung, Y., & Han, J. M. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00504-8 · Cited by 1,021
Papathomas, T. G., Oudijk, L., Persu, A., Gill, A. J., van Nederveen, F. H., Tischler, A. S., Tissier, F., Volante, M., Matías‐Guiu, X., Smid, M., et al. (2015) · Modern Pathology · doi:10.1038/modpathol.2015.41 · Cited by 228
Self-citationCurrent Approaches and Recent Developments in the Management of Head and Neck Paragangliomas
Taïeb, D., Kaliski, A., Boedeker, C. C., Martucci, V. L., Fojo, T., Adler, J. R., & Pacák, K. (2014) · Endocrine Reviews · doi:10.1210/er.2014-1026 · Cited by 169
New treatment strategies for advanced-stage gastrointestinal stromal tumours
Klug, L. R., Khosroyani, H. M., Kent, J. D., & Heinrich, M. C. (2022) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-022-00606-4 · Cited by 148
SDHB-Deficient Cancers: The Role of Mutations That Impair Iron Sulfur Cluster Delivery
Saxena, N., Maio, N., Crooks, D. R., Ricketts, C. J., Yang, Y., Wei, M.-H., Fan, T. W. ‐., Lane, A. N., Sourbier, C., Singh, A., et al. (2015) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djv287 · Cited by 125
Biochemical Assessment of Pheochromocytoma and Paraganglioma
Eisenhofer, G., Pamporaki, C., & Lenders, J. W. M. (2023) · Endocrine Reviews · doi:10.1210/endrev/bnad011 · Cited by 118
Self-citationRichter, S., Gieldon, L., Pang, Y. K., Peitzsch, M., Huynh, T., Letón, R., Viana, B., Ercolino, T., Mangelis, A., Rapizzi, E., et al. (2018) · Genetics in Medicine · doi:10.1038/s41436-018-0106-5 · Cited by 99
Self-citationKadhi, O. A., Melchini, A., Mithen, R. F., & Saha, S. (2017) · Journal of Analytical Methods in Chemistry · doi:10.1155/2017/5391832 · Cited by 94
Oncometabolites: A New Paradigm for Oncology, Metabolism, and the Clinical Laboratory
Collins, R. R. J., Patel, K., Putnam, W. C., Kapur, P., & Rakheja, D. (2017) · Clinical Chemistry · doi:10.1373/clinchem.2016.267666 · Cited by 94
SDHi fungicides: An example of mitotoxic pesticides targeting the succinate dehydrogenase complex
Tête, A., Debizet, K., Imler, J., Tomkiewicz, C., Blanc, É., Barouki, R., Coumoul, X., & Bortoli, S. (2023) · Environment International · doi:10.1016/j.envint.2023.108219 · Cited by 95
Remacha, L., Comino‐Méndez, I., Richter, S., Contreras, L., Currás-Freixes, M., Pita, G., Letón, R., Galarreta, A., Torres‐Pérez, R., Honrado, E., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-2250 · Cited by 98
Self-citationEisenhofer, G., Klink, B., Richter, S., Lenders, J. W. M., & Robledo, M. (2017) · Europe PMC (PubMed Central) · Cited by 84
Self-citationGudgeon, N. H., Munford, H., Bishop, E. L., Hill, J., Fulton-Ward, T., Bending, D., Roberts, J., Tennant, D. A., & Dimeloe, S. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111193 · Cited by 85
Clinical implications of the oncometabolite succinate in SDHx ‐mutation carriers
Eijkelenkamp, K., Osinga, T. E., Links, T. P., & van der Horst‐Schrivers, A. N. A. (2019) · Clinical Genetics · doi:10.1111/cge.13553 · Cited by 78
Döncző, B., & Guttman, A. (2018) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2018.03.065 · Cited by 78
Loss of SDHB Promotes Dysregulated Iron Homeostasis, Oxidative Stress, and Sensitivity to Ascorbate
Goncalves, J., Moog, S., Morin, A., Gentric, G., Müller, S., Morrell, A. P., Kľučková, K., Stewart, T. J., Andoniadou, C. L., Lussey‐Lepoutre, C., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-2936 · Cited by 77
Lussey‐Lepoutre, C., Bellucci, A., Morin, A., Buffet, A., Amar, L., Janin, M., Ottolenghi, C., Zinzindohoué, F., Autret, G., Burnichon, N., et al. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-1576 · Cited by 76
Impériale, A., Moussallieh, F., Roche, P., Battini, S., Çiçek, A. E., Sebag, F. A., Brunaud, L., Barlier, A., Elbayed, K., Loundou, A., et al. (2015) · Neoplasia · doi:10.1016/j.neo.2014.10.010 · Cited by 69
Challenges in Paragangliomas and Pheochromocytomas: from Histology to Molecular Immunohistochemistry
Juhlin, C. C. (2021) · Endocrine Pathology · doi:10.1007/s12022-021-09675-0 · Cited by 69
GEP- NETS UPDATE: Genetics of neuroendocrine tumors
Crona, J., & Skogseid, B. M. (2016) · European Journal of Endocrinology · doi:10.1530/eje-15-0972 · Cited by 71
Metabolic implications of hypoxia and pseudohypoxia in pheochromocytoma and paraganglioma
Kľučková, K., & Tennant, D. A. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2801-6 · Cited by 68
Pheochromocytoma: The First Metabolic Endocrine Cancer
Jochmanová, I., & Pacák, K. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0606 · Cited by 66
Antonio, K. L., Valdez, M. M. N., MERCADO-ASIS, L. B., Taïeb, D., & Pacák, K. (2020) · Gland Surgery · doi:10.21037/gs.2019.10.25 · Cited by 65
MacFarlane, J., Seong, K. C., Bisambar, C., Madhu, B., Allinson, K. S. J., Marker, A. J., Warren, A. Y., Park, S., Giger, O., Challis, B., et al. (2020) · Clinical Endocrinology · doi:10.1111/cen.14289 · Cited by 64
Berends, A. M. A., Eisenhofer, G., Fishbein, L. M., van der Horst‐Schrivers, A. N. A., Kema, I. P., Links, T. P., Lenders, J. W. M., & Kerstens, M. N. (2019) · Cancers · doi:10.3390/cancers11081121 · Cited by 68
Self-citationPheochromocytoma: A Genetic And Diagnostic Update
MERCADO-ASIS, L. B., Wolf, K. I., Jochmanová, I., & Taïeb, D. (2017) · Endocrine Practice · doi:10.4158/ep-2017-0057 · Cited by 58
Precision medicine in pheochromocytoma and paraganglioma: current and future concepts
Björklund, P., Pacák, K., & Crona, J. (2016) · Journal of Internal Medicine · doi:10.1111/joim.12507 · Cited by 59
Epigenetic Mutation of the Succinate Dehydrogenase C Promoter in a Patient With Two Paragangliomas
Richter, S., Klink, B., Nacke, B., de Cubas, A. A., Mangelis, A., Rapizzi, E., Meinhardt, M., Skondra, C. D., Mannelli, M., Robledo, M., et al. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-3856 · Cited by 53
Self-citationDahia, P. L. M., Clifton-Bligh, R. J., Gimenez‐Roqueplo, A., Robledo, M., & Jiménez, C. (2020) · Endocrine Related Cancer · doi:10.1530/erc-19-0435 · Cited by 56
Self-citationBénit, P., Goncalves, J., El‐Khoury, R., Rak, M., Favier, J., Gimenez‐Roqueplo, A., & Rustin, P. (2022) · Biomedicines · doi:10.3390/biomedicines10081788 · Cited by 49
New Biology of Pheochromocytoma and Paraganglioma
Pacák, K. (2022) · Endocrine Practice · doi:10.1016/j.eprac.2022.09.003 · Cited by 44
Impact of LC-MS/MS on the laboratory diagnosis of catecholamine-producing tumors
Eisenhofer, G., Peitzsch, M., & McWhinney, B. C. (2016) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2016.01.027 · Cited by 43
Self-citationThe 3PAs: An Update on the Association of Pheochromocytomas, Paragangliomas, and Pituitary Tumors
Xekouki, P., Brennand, A., Whitelaw, B., Pacák, K., & Stratakis, C. A. (2018) · Hormone and Metabolic Research · doi:10.1055/a-0661-0341 · Cited by 45
Wallace, P. W., Conrad, C., Brückmann, S., Pang, Y. K., Caleiras, E. J., Murakami, M., Korpershoek, E., Zhuang, Z., Rapizzi, E., Kroiß, M., et al. (2020) · The Journal of Pathology · doi:10.1002/path.5472 · Cited by 43
Self-citationThe VHL/HIF Axis in the Development and Treatment of Pheochromocytoma/Paraganglioma
Song, P., Zhang, J., Tan, X., Huang, Y., Xu, J., Silk, N., Zhang, D., Liu, Q., & Jiang, J. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.586857 · Cited by 42
Armstrong, N., Storey, C. M., Noll, S. E., Margulis, K., Soe, M. H., Xu, H., Yeh, B. T., Fishbein, L. M., Kebebew, E., Howitt, B. E., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110453 · Cited by 42
Wojakowska, A., Marczak, Ł., Jelonek, K., Polański, K., Widłak, P., & Pietrowska, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0136902 · Cited by 40
Matlac, D. M., Vanova, K. H., Bechmann, N., Richter, S., Inderhees, J., Ghayee, H. K., Ge, G., Abunimer, L., WESLEY, R. A., Aherrahrou, R., et al. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.589451 · Cited by 40
Self-citationMagnetic resonance spectroscopy of paragangliomas: new insights into in vivo metabolomics
Varoquaux, A. D., Fur, Y. L., Impériale, A., Reyre, A., Montava, M., Fakhry, N., Namer, I. J., Moulin, G., Pacák, K., Guye, M., et al. (2015) · Endocrine Related Cancer · doi:10.1530/erc-15-0246 · Cited by 39
Gieldon, L., William, D., Hackmann, K., Jahn, W., Jahn, A., Wagner, J., Rump, A., Bechmann, N., Nölting, S., Knösel, T., et al. (2019) · Cancers · doi:10.3390/cancers11060809 · Cited by 39
Self-citationEpigenetic and metabolic reprogramming of SDH-deficient paragangliomas
Moog, S., Lussey‐Lepoutre, C., & Favier, J. (2020) · Endocrine Related Cancer · doi:10.1530/erc-20-0346 · Cited by 42
Casey, R. T., McLean, M. A., Madhu, B., Challis, B., ten Hoopen, R., Roberts, T. A., Clark, G. R., Pitfield, D., Simpson, H., Bulusu, V. R., et al. (2018) · JCO Precision Oncology · doi:10.1200/po.17.00191 · Cited by 38
Significance of Alpha-inhibin Expression in Pheochromocytomas and Paragangliomas
Mete, Ö., Pakbaz, S., Lerário, A. M., Giordano, T. J., & Asa, S. L. (2021) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000001715 · Cited by 38
Utility of the succinate:fumarate ratio for assessing SDH dysfunction in different tumor types
Kim, E., Wright, M. J., Sioson, L., Novos, T., Gill, A. J., Benn, D. E., White, C., Dwight, T., & Clifton-Bligh, R. J. (2016) · Molecular Genetics and Metabolism Reports · doi:10.1016/j.ymgmr.2016.12.006 · Cited by 38
Structural and functional consequences of succinate dehydrogenase subunit B mutations
Kim, E., Rath, E. M., Tsang, V., Duff, A. P., Robinson, B. G., Church, W. B., Benn, D. E., Dwight, T., & Clifton-Bligh, R. J. (2015) · Endocrine Related Cancer · doi:10.1530/erc-15-0099 · Cited by 39
Circulating Metabolites and Survival Among Patients With Pancreatic Cancer
Yuan, C., Clish, C. B., Wu, C. H., Mayers, J. R., Kraft, P. L., Townsend, M. K., Zhang, M., Tworoger, S. S., Bao, Y., Qian, Z. R., et al. (2016) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djv409 · Cited by 37
The microenvironment induces collective migration in SDHB-silenced mouse pheochromocytoma spheroids
D’Antongiovanni, V., Martinelli, S., Richter, S., Canu, L., Guasti, D., Mello, T., Romagnoli, P., Pacák, K., Eisenhofer, G., Mannelli, M., et al. (2017) · Endocrine Related Cancer · doi:10.1530/erc-17-0212 · Cited by 37
Self-citationMutant IDH1 Differently Affects Redox State and Metabolism in Glial Cells of Normal and Tumor Origin
Biedermann, J., Preussler, M., Conde, M., Peitzsch, M., Richter, S., Wiedemuth, R., Abou‐El‐Ardat, K., Krüger, A., Meinhardt, M., Schackert, G., et al. (2019) · Cancers · doi:10.3390/cancers11122028 · Cited by 36
Self-citationLussey‐Lepoutre, C., Bellucci, A., Burnichon, N., Amar, L., Buffet, A., Drossart, T., Fontaine, S., Clémеnt, O., Bénit, P., Rustin, P., et al. (2019) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-019-04633-9 · Cited by 34
The Evolving Role of Succinate in Tumor Metabolism: An 18F-FDG–Based Study
Garrigue, P., Bodin-Hullin, A., Balasse, L., Fernandez-Sauze, S., Essamet, W., Dignat‐George, F., Pacák, K., Guillet, B. A., & Taïeb, D. (2017) · Journal of Nuclear Medicine · doi:10.2967/jnumed.117.192674 · Cited by 33
Adrenocortical carcinoma and succinate dehydrogenase gene mutations: an observational case series
Else, T., Lerário, A. M., Everett, J. N., Haymon, L., Wham, D., Mullane, M. P., Wilson, T. L. S., Rainville, I. R., Rana, H. Q., Worth, A. J., et al. (2017) · European Journal of Endocrinology · doi:10.1530/eje-17-0358 · Cited by 33
Intratumoral heterogeneity of MYC drives medulloblastoma metastasis and angiogenesis
Qin, N., Paisana, E., Langini, M., Picard, D. J., Malzkorn, B., Custódia, C., Cascão, R., Meyer, F.-D., Blümel, L., Göbbels, S., et al. (2022) · Neuro-Oncology · doi:10.1093/neuonc/noac068 · Cited by 33
Self-citationOxygen Concentration Controls Epigenetic Effects in Models of Familial Paraganglioma
Her, Y. F., Nelson-Holte, M. H., & Maher, L. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127471 · Cited by 34
Pheochromocytomas and Paragangliomas: Bypassing Cellular Respiration
Cascón, A., Remacha, L., Calsina, B., & Robledo, M. (2019) · Cancers · doi:10.3390/cancers11050683 · Cited by 33
Self-citationSater, Z. A., Jha, A., Hamimi, A., Mandl, A., Hartley, I. R., Gubbi, S., Patel, M. A., Gonzales, M., Taïeb, D., Civelek, A. C., et al. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgz314 · Cited by 31
Richter, S., D’Antongiovanni, V., Martinelli, S., Bechmann, N., Riverso, M., Poitz, D. M., Pacák, K., Eisenhofer, G., Mannelli, M., & Rapizzi, E. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2907-x · Cited by 30
Self-citationThe Immune Landscape of Pheochromocytoma and Paraganglioma: Current Advances and Perspectives
Uher, O., Vanova, K. H., Taïeb, D., Calsina, B., Robledo, M., Clifton-Bligh, R. J., & Pacák, K. (2024) · Endocrine Reviews · doi:10.1210/endrev/bnae005 · Cited by 31
Self-citationPheochromocytoma: Gasping for Air
Jochmanová, I., Zhuang, Z., & Pacák, K. (2015) · Hormones and Cancer · doi:10.1007/s12672-015-0231-4 · Cited by 30
Succinate dehydrogenase and MYC-associated factor X mutations in pituitary neuroendocrine tumours
Loughrey, P. B., Roncaroli, F., Healy, E. G., Weir, P., Madhu, B., Casey, R. T., Hunter, S. J., & Korbonits, M. (2022) · Endocrine Related Cancer · doi:10.1530/erc-22-0157 · Cited by 28
Liu, Z., Ma, J., Jiménez, C., & Zhang, M. (2021) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000001768 · Cited by 28
Yu, S., Zhou, W., Yu, J., Li, M., Zhang, S., Jiang, X., Wang, H., Ma, X., Zou, Y., Wang, D., et al. (2022) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-022-03984-x · Cited by 28
Tumour microenvironment in pheochromocytoma and paraganglioma
Martinelli, S., Amore, F., Canu, L., Maggi, M., & Rapizzi, E. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1137456 · Cited by 26
Self-citationRole of microenvironment on neuroblastoma SK-N-AS SDHB-silenced cell metabolism and function
Rapizzi, E., Fucci, R., Giannoni, E., Canu, L., Richter, S., Cirri, P., & Mannelli, M. (2015) · Endocrine Related Cancer · doi:10.1530/erc-14-0479 · Cited by 26
Self-citationFéral, C. C., Tissot, F. S., Tosello, L., Fakhry, N., Sebag, F. A., Pacák, K., & Taïeb, D. (2016) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-016-3586-z · Cited by 26
Succinate: A Serum Biomarker of SDHB-Mutated Paragangliomas and Pheochromocytomas
Lamy, C., Tissot, H., Faron, M., Baudin, É., Lamartina, L., Pradon, C., Ghuzlan, A. A., Leboulleux, S., Perfettini, J., Paci, A., et al. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac474 · Cited by 25
Casey, R. T., ten Hoopen, R., Ochoa, E., Challis, B., Whitworth, J., Smith, P., Martín, J., Clark, G. R., Rodger, F., Maranian, M. J., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-46124-9 · Cited by 24
Fliedner, S. M. J., Brabant, G. E., & Lehnert, H. (2018) · Cell and Tissue Research · doi:10.1007/s00441-017-2760-3 · Cited by 22
Adrenal Hormone Interactions and Metabolism: A Single Sample Multi-Omics Approach
Bechmann, N., Watts, D., Steenblock, C., Wallace, P. W., Schürmann, A., Bornstein, S. R., Wielockx, B., Eisenhofer, G., & Peitzsch, M. (2021) · Hormone and Metabolic Research · doi:10.1055/a-1440-0278 · Cited by 21
Self-citationRodent models of pheochromocytoma, parallels in rodent and human tumorigenesis
Lussey‐Lepoutre, C., Buffet, A., Morin, A., Goncalves, J., & Favier, J. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2797-y · Cited by 23
Targeting pheochromocytoma/paraganglioma with polyamine inhibitors
Rai, S. K., Bril, F., Hatch, H. M., Xu, Y., Shelton, L. M., Kalavalapalli, S., Click, A., Lee, D., Beecher, C., Kirby, A., et al. (2020) · Metabolism · doi:10.1016/j.metabol.2020.154297 · Cited by 20
Self-citationLoss of sdhb in zebrafish larvae recapitulates human paraganglioma characteristics
Dona, M., Waaijers, S., Richter, S., Eisenhofer, G., Korving, J., Kamel, S. M., Bakkers, J., Rapizzi, E., Rodenburg, R. J., Zethof, J., et al. (2020) · Endocrine Related Cancer · doi:10.1530/erc-20-0308 · Cited by 21
Self-citationWang, Y., Liu, B., Li, F., Zhang, Y., Gao, X., Wang, Y., & Zhou, H. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1274239 · Cited by 18
Fliedner, S. M. J., Shankavaram, U. T., Marzouca, G., ELKAHLOUN, A. G., Jochmanová, I., Därr, R., Linehan, W. M., Timmers, H. J. L. M., Tischler, A. S., Papaspyrou, K., et al. (2016) · Neoplasia · doi:10.1016/j.neo.2016.07.008 · Cited by 20
Self-citationMartinelli, S., Riverso, M., Mello, T., Amore, F., Parri, M., Simeone, I., Mannelli, M., Maggi, M., & Rapizzi, E. (2022) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2022.111594 · Cited by 17
Self-citationClinical and molecular markers guide the genetics of pheochromocytoma and paraganglioma
Cascón, A., & Robledo, M. (2024) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2024.189141 · Cited by 16
Self-citationMetabolomics in paraganglioma: applications and perspectives from genetics to therapy
Richter, S., Garrett, T. J., Bechmann, N., Clifton-Bligh, R. J., & Ghayee, H. K. (2023) · Endocrine Related Cancer · doi:10.1530/erc-22-0376 · Cited by 16
Self-citationSousa, S. M. C. D., Toubia, J., Hardy, T., Feng, J., Wang, P. P.-S., SCHREIBER, A. W., Geoghegan, J. M., Hall, R. K., Rawlings, L. H., Buckland, M. E., et al. (2020) · Journal of the Endocrine Society · doi:10.1210/jendso/bvaa071 · Cited by 16
Novel methods in adrenal research: a metabolomics approach
Papathomas, T. G., Sun, N., Chortis, V., Taylor, A. E., Arlt, W., Richter, S., Eisenhofer, G., Ruiz-Babot, G., Guasti, L., & Walch, A. K. (2019) · Histochemistry and Cell Biology · doi:10.1007/s00418-019-01772-w · Cited by 14
Self-citationBuszewska‐Forajta, M., Patejko, M., Macioszek, S., Sigorski, D., Iżycka‐Świeszewska, E., & Markuszewski, M. J. (2019) · Chromatographia · doi:10.1007/s10337-019-03769-y · Cited by 14
Pheochromocytoma/paraganglioma preclinical models: which to use and why?
Martinelli, S., Maggi, M., & Rapizzi, E. (2020) · Endocrine Connections · doi:10.1530/ec-20-0472 · Cited by 14
Self-citation15 YEARS OF PARAGANGLIOMA: Metabolism and pheochromocytoma/paraganglioma
Mannelli, M., Rapizzi, E., Fucci, R., Canu, L., Ercolino, T., Luconi, M., & Young, W. F. (2015) · Endocrine Related Cancer · doi:10.1530/erc-15-0215 · Cited by 15
Self-citationYamamoto, T., Sato, K., Yamaguchi, M., Mitamura, K., & Taga, A. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.10.072 · Cited by 14
Metabolomics in the Diagnosis of Pheochromocytoma and Paraganglioma
Dwight, T., Kim, E., Novos, T., & Clifton-Bligh, R. J. (2019) · Hormone and Metabolic Research · doi:10.1055/a-0926-3790 · Cited by 14
Lee, S., Needleman, L., Park, J. R., Schugar, R. C., Guo, Q., Ford, J. M., & Annes, J. P. (2025) · Journal of Clinical Investigation · doi:10.1172/jci198165 · Cited by 14
Plasma Metabolome Profiling for the Diagnosis of Catecholamine Producing Tumors
März, J., Kurlbaum, M., Roche-Lancaster, O., Deutschbein, T., Peitzsch, M., Prehn, C. P., Weismann, D., Robledo, M., Adamski, J., Faßnacht, M., et al. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.722656 · Cited by 12
Self-citationQin, N., Paisana, E., Picard, D. J., Leprivier, G., Langini, M., Custódia, C., Cascão, R., Conrad, C., Peitzsch, M., Stefanski, A., et al. (2023) · Journal of Neuro-Oncology · doi:10.1007/s11060-023-04508-y · Cited by 11
Self-citationMartins, R. G., Gonçalves, L. G., Cunha, N., & Bugalho, M. J. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2019-01101 · Cited by 11
Toward Systems-Level Metabolic Analysis in Endocrine Disorders and Cancer
Lakhani, A., Kang, D. H., Kang, Y. E., & Park, J. O. (2023) · Endocrinology and Metabolism · doi:10.3803/enm.2023.1814 · Cited by 11
Marden, J. H., Langford, E. A., Robertson, M. A., & Fescemyer, H. W. (2020) · Evolution · doi:10.1111/evo.14095 · Cited by 11
Gregorio, E. D., Miolo, G., Saorin, A., Steffan, A., & Corona, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115574 · Cited by 11
Hart, M. L., Sokolov, D., Danquah, S., Zheng, E., Doan, A. D., Davidsen, K., MacPherson, D. P., & Sullivan, L. B. (2026) · Nature Metabolism · doi:10.1038/s42255-026-01524-w · Cited by 10
Bancel, L.-P., Masso, V., Dessein, A., Aubert, S., Leteurtre, E., Coppin, L., Odou, M., Cao, C. D., Cardot-Bauters, C., & Pigny, P. (2023) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgad109 · Cited by 10
Clinical and biochemical footprints of inherited metabolic diseases. VIII. Neoplasias
Serrano, T. J., Blau, N., & Ferreira, C. R. (2022) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2022.03.011 · Cited by 9
Asensio, A. F., Álvarez-González, E., Rodríguez, A., Sierra, L. M., & Blanco‐González, E. (2021) · Analytica Chimica Acta · doi:10.1016/j.aca.2021.338646 · Cited by 10
Lamy, C., Mansard, C., Blondel, L., Mercier, L., Paci, A., & Broutin, S. (2021) · Journal of Chromatography B · doi:10.1016/j.jchromb.2021.123085 · Cited by 8
Gabiache, G., Zadro, C., Rozenblum, L., Vezzosi, D., Mouly, C., Thoulouzan, M., Guimbaud, R., Otal, P., Dierickx, L., Rousseau, H., et al. (2023) · Cancers · doi:10.3390/cancers15184666 · Cited by 8
Identification of Succinate Dehydrogenase Gene Variant Carriers by Blood Biomarkers
Gebhardt, M., Kunath, C., Fröbel, D., Funk, A. M., Peitzsch, M., Nölting, S., Deutschbein, T., Januszewicz, A., Timmers, H. J. L. M., Robledo, M., et al. (2024) · Journal of the Endocrine Society · doi:10.1210/jendso/bvae142 · Cited by 7
Self-citationSvendsen, L. K., Rasmussen, Å. K., Klose, M., Krogh, J., & Feldt‐Rasmussen, U. (2025) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaf584 · Cited by 6
van den Berg, M. F., Bechmann, N., Kooistra, H. S., van Wolferen, M. E., Timmermans‐Sprang, E. P. M., Peitzsch, M., & Galac, S. (2024) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.17148 · Cited by 6
Self-citationPetrák, J., Tevosian, S. G., Richter, S., & Ghayee, H. K. (2024) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2024.101935 · Cited by 5
Self-citation
Metadata
- Authors
- Richter, S., Peitzsch, M., Rapizzi, E., Lenders, J. W., Qin, N., de Cubas, A. A., Schiavi, F., Rao, J. U., Beuschlein, F., Quinkler, M., Timmers, H. J., Opocher, G., Mannelli, M., Pacak, K., Robledo, M., & Eisenhofer, G.
- Affiliations
- University Hospital Carl Gustav Carus (DE)
- University of Florence (IT)
- Radboud University Medical Center (NL)
- Hereditary Endocrine Cancer Group (A.A.C., M.R.), CNIO, Madrid, Spain
- Istituto Oncologico Veneto (IT)
- LMU Klinikum (DE)
- Charité – Universitätsmedizin Berlin (DE)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (K.P.), National Institutes of Health, 10 Center Drive, MSC-1109, Bethesda, Maryland 20892-1109
- Spanish National Cancer Research Centre (ES)
- Corresponding author
- Richter, Susan
- ORCID
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2014-10-01
- Volume
- 99
- Issue
- 10
- Pages
- 3903-3911
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- PMC
- PMC4184070
- OpenAlex
- W2116263600
- Cited by
- 135
- References
- 35
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 6 · 2023: 16 · 2022: 17 · 2021: 15 · 2020: 14 · 2019: 11 · 2018: 8 · 2017: 12 · 2016: 10 · 2015: 14 · 2014: 1
- FWCI
- 12.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Florence Research (University of Florence) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Adrenal and Paraganglionic Tumors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Metabolism and Genetic Disorders
- Health Sciences › Medicine › Oncology › Neuroblastoma Research and Treatments
- Keywords
- pheochromocytoma, paraganglioma, succinate dehydrogenase deficiency, SDHx mutations, Krebs cycle metabolites, SDHB mutation, metastasis, mutation detection, isocitrate, cis-aconitate
- MeSH terms
- Adolescent, Adrenal Gland Neoplasms, Adult, Aged, Citric Acid Cycle, Female, Follow-Up Studies, Fumarates, Humans, Male, Metabolic Diseases, Middle Aged, Paraganglioma, Pheochromocytoma, Sensitivity and Specificity, Succinate Dehydrogenase, Germ-Line Mutation, Succinic Acid, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
