I-131 metaiodobenzylguanidine therapy is a significant treatment option for pheochromocytoma and paraganglioma

Abstract

Aim Pheochromocytomas and paragangliomas (PPGLs) are rare neuroendocrine tumours of chromaffin cells. Several modalities are currently available to treat patients with PPGL. These treatment modalities include surgery, chemotherapy, molecular targeted therapy and radiopharmaceuticals.

Methods I-131 metaiodobenzylguanidine (mIBG), a classic radiopharmaceutical, can be taken up through specific receptors and sited into many, but not all, PPGL cells.

Results Many studies have investigated the efficacy and toxicity of I-131 mIBG therapy. These studies reported significant results in terms of objective, hormonal and symptomatic responses as well as tolerable toxicities in patients.

Conclusion This article reviews the reported experiences of patients who underwent I-131 mIBG therapy for PPGL with a focus on functions and deficiencies of the therapy.

Zusammenfassung

Ziel Phäochromozytome und Paragangliome (PPGL) sind seltene neuroendokrine Tumoren der chromaffinen Zellen. Für die Behandlung von Patienten mit PPGL stehen derzeit mehrere Modalitäten zur Verfügung. Zu diesen Behandlungsmethoden gehören Chirurgie, Chemotherapie, molekulare zielgerichtete Therapie und Radiopharmaka.

Methoden I-131-Metaiodobenzylguanidin (mIBG), ein klassisches Radiopharmakon, kann über spezifische Rezeptoren aufgenommen werden und in vielen, aber nicht allen PPGL-Zellen lokalisiert werden.

Ergebnisse Viele Studien haben die Wirksamkeit und Toxizität der Therapie mit I-131-mIBG untersucht. Diese Studien berichteten signifikante Daten in Bezug auf objektive, hormonelle und symptomatische Reaktionen sowie tolerierbare Toxizitäten bei Patienten.

Schlussfolgerung Dieser Artikel gibt einen Überblick über die berichteten Erfahrungen von Patienten, die sich einer I-131-mIBG-Therapie für PPGL unterzogen haben, wobei der Schwerpunkt auf den Funktionen und Mängeln der Therapie liegt.

Schlüsselwörter

Phäochromozytome und Paragangliome - Metaiodbenzylguanidin - neuroendokrine Tumore

Keywords

Pheochromocytomas and paragangliomas - metaiodobenzylguanidine - neuroendocrine tumours

Publication History

Received: 10 August 2021

Accepted after revision: 22 January 2022

Article published online:
03 June 2022

• References

• 1 Lenders JW, Eisenhofer G, Mannelli M. et al. Phaeochromocytoma. LANCET 2005; 366: 665-675 DOI: 10.1097/HJH.0000000000002438. (PMID: 32412940)
• 2 Eisenhofer G, Peitzsch M. Laboratory evaluation of pheochromocytoma and paraganglioma. CLIN CHEM 2014; 60: 1486-1499 DOI: 10.1373/clinchem.2014.224832. (PMID: 25332315)
• 3 Garcia-Carbonero R, Matute TF, Mercader-Cidoncha E. et al. Multidisciplinary practice guidelines for the diagnosis, genetic counseling and treatment of pheochromocytomas and paragangliomas. CLIN TRANSL ONCOL 2021; 23: 1995-2019
• 4 Kölby L, Bernhardt P, Levin-Jakobsen AM. et al. Uptake of meta-iodobenzylguanidine in neuroendocrine tumours is mediated by vesicular monoamine transporters. Br J Cancer 2003; 89: 1383-1388 DOI: 10.1038/sj.bjc.6601276. (PMID: 14520475)
• 5 Gaze MN, Huxham IM, Mairs RJ. et al. Intracellular localization of metaiodobenzyl guanidine in human neuroblastoma cells by electron spectroscopic imaging. INT J CANCER 1991; 47: 875-880 DOI: 10.1002/ijc.2910470615. (PMID: 2010230)
• 6 Giammarile F, Chiti A, Lassmann M. et al. EANM procedure guidelines for 131I-meta-iodobenzylguanidine (131I-mIBG) therapy. Eur J Nucl Med Mol Imaging 2008; 35: 1039-1047 DOI: 10.1007/s00259-008-0715-3. (PMID: 18274745)
• 7 Fukuoka M, Taki J, Mochizuki T. et al. Comparison of diagnostic value of I-123 MIBG and high-dose I-131 MIBG scintigraphy including incremental value of SPECT/CT over planar image in patients with malignant pheochromocytoma/paraganglioma and neuroblastoma. CLIN NUCL MED 2011; 36: 1-7 DOI: 10.1097/RLU.0b013e3181feeb5e. (PMID: 21157198)
• 8 Taïeb D, Hicks RJ, Hindié E. 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 2019; 46: 2112-2137 DOI: 10.1007/s00259-019-04398-1. (PMID: 31254038)
• 9 Ilias I, Pacak K. Current approaches and recommended algorithm for the diagnostic localization of pheochromocytoma. J Clin Endocrinol Metab 2004; 89: 479-491 DOI: 10.1210/jc.2003-031091. (PMID: 14764749)
• 10 Sisson JC, Shulkin BL. Nuclear medicine imaging of pheochromocytoma and neuroblastoma. Q J Nucl Med 1999; 43: 217-223 (PMID: 10568137)
• 11 van der Harst E, de Herder WW, Bruining HA. et al. (123)I]metaiodobenzylguanidine and [(111)In. J Clin Endocrinol Metab 2001; 86: 685-693 DOI: 10.1210/jcem.86.2.7238. (PMID: 11158032)
• 12 Wiseman GA, Pacak K, O'Dorisio MS. et al. Usefulness of 123I-MIBG scintigraphy in the evaluation of patients with known or suspected primary or metastatic pheochromocytoma or paraganglioma: results from a prospective multicenter trial. J NUCL MED 2009; 50: 1448-1454 DOI: 10.2967/jnumed.108.058701. (PMID: 19690028)
• 13 Fonte JS, Robles JF, Chen CC. et al. False-negative ¹²³I-MIBG SPECT is most commonly found in SDHB-related pheochromocytoma or paraganglioma with high frequency to develop metastatic disease. Endocr Relat Cancer 2012; 19: 83-93 DOI: 10.1530/ERC-11-0243. (PMID: 22167067)
• 14 Janssen I, Chen CC, Taieb D. et al. 68Ga-DOTATATE PET/CT in the localization of head and neck paragangliomas compared with other functional imaging modalities and CT/MRI. J NUCL MED 2016; 57: 186-191 DOI: 10.2967/jnumed.115.161018. (PMID: 26564322)
• 15 Shapiro B, Sisson JC, Eyre P. et al. 131I-MIBG--a new agent in diagnosis and treatment of pheochromocytoma. CARDIOLOGY 1985; 72 (Suppl. 01) 137-142 DOI: 10.1159/000173960. (PMID: 4053121)
• 16 Rutherford MA, Rankin AJ, Yates TM. et al. Management of metastatic phaeochromocytoma and paraganglioma: use of iodine-131-meta-iodobenzylguanidine therapy in a tertiary referral centre. QJM 2015; 108: 361-368 DOI: 10.1093/qjmed/hcu208. (PMID: 25267727)
• 17 Yoshinaga K, Oriuchi N, Wakabayashi H. et al. Effects and safety of ¹³¹I-metaiodobenzylguanidine (MIBG) radiotherapy in malignant neuroendocrine tumors: results from a multicenter observational registry. ENDOCR J 2014; 61: 1171-1180 DOI: 10.1507/endocrj.EJ14-0211. (PMID: 25214026)
• 18 Wakabayashi H, Taki J, Inaki A. et al. Prognostic values of initial responses to low-dose (131)I-MIBG therapy in patients with malignant pheochromocytoma and paraganglioma. ANN NUCL MED 2013; 27: 839-846 DOI: 10.1007/s12149-013-0755-z. (PMID: 23864328)
• 19 Wakabayashi H, Inaki A, Yoshimura K. et al. A phase I clinical trial for [(131)I]meta-iodobenzylguanidine therapy in patients with refractory pheochromocytoma and paraganglioma. Sci Rep 2019; 9: 7625 DOI: 10.1038/s41598-019-43880-6. (PMID: 31110198)
• 20 Shilkrut M, Bar-Deroma R, Bar-Sela G. et al. Low-dose iodine-131 metaiodobenzylguanidine therapy for patients with malignant pheochromocytoma and paraganglioma: single center experience. Am J Clin Oncol 2010; 33: 79-82 DOI: 10.1097/COC.0b013e31819e2c28. (PMID: 19704370)
• 21 Shapiro B, Sisson JC, Wieland DM. et al. Radiopharmaceutical therapy of malignant pheochromocytoma with [131I]metaiodobenzylguanidine: results from ten years of experience. J Nucl Biol Med 1991; 35: 269-276 (PMID: 1823834)
• 22 Castellani MR, Seghezzi S, Chiesa C. et al. (131)I-MIBG treatment of pheochromocytoma: low versus intermediate activity regimens of therapy. Q J Nucl Med Mol Imaging 2010; 54: 100-113 (PMID: 20168292)
• 23 Safford SD, Coleman RE, Gockerman JP. et al. Iodine -131 metaiodobenzylguanidine is an effective treatment for malignant pheochromocytoma and paraganglioma. SURGERY 2003; 134: 956-963 DOI: 10.1016/s0039-6060(03)00426-4. (PMID: 14668728)
• 24 Gedik GK, Hoefnagel CA, Bais E. et al. 131I-MIBG therapy in metastatic phaeochromocytoma and paraganglioma. Eur J Nucl Med Mol Imaging 2008; 35: 725-733 DOI: 10.1007/s00259-007-0652-6. (PMID: 18071700)
• 25 Thorpe MP, Kane A, Zhu J. et al. Long-term outcomes of 125 patients with metastatic pheochromocytoma or paraganglioma treated with 131-I MIBG. J Clin Endocrinol Metab 2020; 105 (03) dgz074 DOI: 10.1210/clinem/dgz074. (PMID: 31614368)
• 26 Fitzgerald PA, Goldsby RE, Huberty JP. et al. Malignant pheochromocytomas and paragangliomas: a phase II study of therapy with high-dose 131I-metaiodobenzylguanidine (131I-MIBG). Ann N Y Acad Sci 2006; 1073: 465-490 DOI: 10.1196/annals.1353.050. (PMID: 17102115)
• 27 Rose B, Matthay KK, Price D. et al. High-dose 131I-metaiodobenzylguanidine therapy for 12 patients with malignant pheochromocytoma. CANCER-AM CANCER SOC 2003; 98: 239-248
• 28 Gonias S, Goldsby R, Matthay KK. et al. Phase II study of high-dose [131I]metaiodobenzylguanidine therapy for patients with metastatic pheochromocytoma and paraganglioma. J CLIN ONCOL 2009; 27: 4162-4168 DOI: 10.1200/JCO.2008.21.3496. (PMID: 19636009)
• 29 Loh KC, Fitzgerald PA, Matthay KK. et al. The treatment of malignant pheochromocytoma with iodine-131 metaiodobenzylguanidine (131I-MIBG): a comprehensive review of 116 reported patients. J ENDOCRINOL INVEST 1997; 20: 648-658 DOI: 10.1007/BF03348026. (PMID: 9492103)
• 30 Buscombe JR, Cwikla JB, Caplin ME. et al. Long-term efficacy of low activity meta-[131I]iodobenzylguanidine therapy in patients with disseminated neuroendocrine tumours depends on initial response. NUCL MED COMMUN 2005; 26: 969-976 DOI: 10.1097/01.mnm.0000184941.06123.b9. (PMID: 16208174)
• 31 van Hulsteijn LT, Niemeijer ND, Dekkers OM. et al. (131)I-MIBG therapy for malignant paraganglioma and phaeochromocytoma: systematic review and meta-analysis. Clin Endocrinol (Oxf) 2014; 80: 487-501 DOI: 10.1111/cen.12341. (PMID: 24118038)
• 32 Hartley A, Spooner D, Brunt AM. Management of malignant phaeochromocytoma: a retrospective review of the use of MIBG and chemotherapy in the West Midlands. Clin Oncol (R Coll Radiol) 2001; 13: 361-366 DOI: 10.1053/clon.2001.9290. (PMID: 11716230)
• 33 Sisson JC, Shapiro B, Shulkin BL. et al. Treatment of malignant pheochromocytomas with 131-I metaiodobenzylguanidine and chemotherapy. Am J Clin Oncol 1999; 22: 364-370 DOI: 10.1097/00000421-199908000-00008. (PMID: 10440191)
• 34 Makis W, McCann K, McEwan AJ. et al. 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 2016; 41: 204-206
• 35 Vogel J, Atanacio AS, Prodanov T. et al. External beam radiation therapy in treatment of malignant pheochromocytoma and paraganglioma. FRONT ONCOL 2014; 4: 166 DOI: 10.3389/fonc.2014.00166. (PMID: 25019060)
• 36 Fishbein L, Bonner L, Torigian DA. et al. External beam radiation therapy (EBRT) for patients with malignant pheochromocytoma and non-head and -neck paraganglioma: combination with 131I-MIBG. HORM METAB RES 2012; 44: 405-410 DOI: 10.1055/s-0032-1308992. (PMID: 22566196)
• 37 Porter AT, McEwan AJ, Powe JE. et al. Results of a randomized phase-III trial to evaluate the efficacy of strontium-89 adjuvant to local field external beam irradiation in the management of endocrine resistant metastatic prostate cancer. Int J Radiat Oncol Biol Phys 1993; 25: 805-813 DOI: 10.1016/0360-3016(93)90309-j. (PMID: 8478230)
• 38 Spetz J, Dalmo J, Nilsson O. et al. Specific binding and uptake of 131I-MIBG and 111In-octreotide in metastatic paraganglioma--tools for choice of radionuclide therapy. HORM METAB RES 2012; 44: 400-404 DOI: 10.1055/s-0032-1311603. (PMID: 22566195)
• 39 Forssell-Aronsson E, Bernhardt P, Wängberg B. et al. Aspects on radionuclide therapy in malignant pheochromocytomas. Ann N Y Acad Sci 2006; 1073: 498-504 DOI: 10.1196/annals.1353.052. (PMID: 17102117)
• 40 Hope TA, Bodei L, Chan JA. et al. NANETS/SNMMI Consensus Statement on Patient Selection and Appropriate Use of (177)Lu-DOTATATE Peptide Receptor Radionuclide Therapy. J NUCL MED 2020; 61: 222-227 DOI: 10.2967/jnumed.119.240911. (PMID: 32015164)
• 41 Lumbroso J, Schlumberger M, Tenenbaum F. et al. [131I]metaiodobenzylguanidine therapy in 20 patients with malignant pheochromocytoma. J Nucl Biol Med 1991; 35: 288-291 (PMID: 1823838)
• 42 Sze WC, Grossman AB, Goddard I. et al. Sequelae and survivorship in patients treated with (131)I-MIBG therapy. Br J Cancer 2013; 109: 565-572 DOI: 10.1038/bjc.2013.365. (PMID: 23860527)
• 43 Kayano D, Kinuya S. Current Consensus on I-131 MIBG Therapy. Nucl Med Mol Imaging 2018; 52: 254-265 DOI: 10.1007/s13139-018-0523-z. (PMID: 30100938)
• 44 Carrasquillo JA, Pandit-Taskar N, Chen CC. I-131 Metaiodobenzylguanidine Therapy of Pheochromocytoma and Paraganglioma. SEMIN NUCL MED 2016; 46: 203-214 DOI: 10.1053/j.semnuclmed.2016.01.011. (PMID: 27067501)
• 45 Mukherjee JJ, Kaltsas GA, Islam N. et al. Treatment of metastatic carcinoid tumours, phaeochromocytoma, paraganglioma and medullary carcinoma of the thyroid with (131)I-meta-iodobenzylguanidine [(131)I-mIBG]. Clin Endocrinol (Oxf) 2001; 55: 47-60 DOI: 10.1046/j.1365-2265.2001.01309.x. (PMID: 11453952)
• 46 Pryma DA, Chin BB, Noto RB. et al. Efficacy and Safety of High-Specific-Activity (131)I-MIBG Therapy in Patients with Advanced Pheochromocytoma or Paraganglioma. J NUCL MED 2019; 60: 623-630 DOI: 10.2967/jnumed.118.217463. (PMID: 30291194)
• 47 Noto RB, Pryma DA, Jensen J. et al. Phase 1 study of high-specific-activity I-131 MIBG for metastatic and/or recurrent pheochromocytoma or paraganglioma. J Clin Endocrinol Metab 2018; 103: 213-220 DOI: 10.1210/jc.2017-02030. (PMID: 29099942)
• 48 Coleman RE, Stubbs JB, Barrett JA. et al. Radiation dosimetry, pharmacokinetics, and safety of ultratrace Iobenguane I-131 in patients with malignant pheochromocytoma/paraganglioma or metastatic carcinoid. Cancer Biother Radiopharm 2009; 24: 469-475 DOI: 10.1089/cbr.2008.0584. (PMID: 19694582)
• 49 Buckley SE, Chittenden SJ, Saran FH. et al. Whole-body dosimetry for individualized treatment planning of 131I-MIBG radionuclide therapy for neuroblastoma. J NUCL MED 2009; 50: 1518-1524 DOI: 10.2967/jnumed.109.064469. (PMID: 19713562)
• 50 Matthay KK, Panina C, Huberty J. et al. Correlation of tumor and whole-body dosimetry with tumor response and toxicity in refractory neuroblastoma treated with (131)I-MIBG. J NUCL MED 2001; 42: 1713-1721 (PMID: 11696644)
• 51 Gaze MN, Chang YC, Flux GD. et al. Feasibility of dosimetry-based high-dose 131I-meta-iodobenzylguanidine with topotecan as a radiosensitizer in children with metastatic neuroblastoma. Cancer Biother Radiopharm 2005; 20: 195-199 DOI: 10.1089/cbr.2005.20.195. (PMID: 15869455)
• 52 Flux GD, Guy MJ, Papavasileiou P. et al. Absorbed dose ratios for repeated therapy of neuroblastoma with I-131 mIBG. Cancer Biother Radiopharm 2003; 18: 81-87 DOI: 10.1089/108497803321269359. (PMID: 12667311)
• 53 Gear J, Chiesa C, Lassmann M. et al. EANM Dosimetry Committee series on standard operational procedures for internal dosimetry for (131)I mIBG treatment of neuroendocrine tumours. EJNMMI Phys 2020; 7: 15 DOI: 10.1186/s40658-020-0282-7. (PMID: 32144574)