, Volume 59, Issue 3, pp 547–554 | Cite as

Prevention of serious skeletal-related events by interventional radiology techniques in patients with malignant paraganglioma and pheochromocytoma

  • Guillaume GravelEmail author
  • Sophie Leboulleux
  • Lambros Tselikas
  • Flora Fassio
  • Mohamed Berraf
  • Amandine Berdelou
  • Bakar Ba
  • Segolene Hescot
  • Julien Hadoux
  • Martin Schlumberger
  • Abir Al Ghuzlan
  • France Nguyen
  • Mathieu Faron
  • Thierry de Baere
  • Eric Baudin
  • Frederic Deschamps
Original Article



Bone metastases (BM) and skeletal-related events (SRE) are frequent in patients with malignant pheochromocytoma and paraganglioma (PPM) and the best modality of prevention unknown. The role of interventional radiology (IR) techniques for the prevention of SRE in the multidisciplinary management of malignant PPM has not been evaluated in that setting.


Single referral center retrospective review of all patients with malignant PPM with BM from 2000 to 2016. The primary endpoint was the time to first serious SRE (TTSRE). At time of inclusion, patients with high bone tumor burden disease were defined as those having more than five BM with the biggest exceeding 2 cm (Group A) and patients with moderate bone tumor burden disease were defined as those having five or less BM or no BM exceeding 2 cm (Group B).


A total of 28 patients were included in this study. Thirteen were treated by IR techniques for prevention of first serious SRE. After a median follow-up of 48.2 months, the median TTSRE was not reached in patients treated by IR techniques and was 26.0 months in patients without IR procedures (p = .058). When comparing patients in group B, TTSRE was significantly higher in patients treated by IR (10 patients) when compared to patients without IR procedures (12 patients) (p = .021).


IR techniques may help to delay the occurrence of first serious SRE in patients with malignant PPM with moderate bone tumor burden disease. Prospective studies are expected to confirm these results.


Paraganglioma Pheochromocytoma Bone metastases Interventional radiology Skeletal-related events 



Bone metastasis


Skeletal-related event


Paragangliomas and pheochromocytomas


Interventional radiology


Time to first serious SRE




Positron emission tomography


Computed tomography


Disease-free interval


Last follow-up




Percutaneous vertebroplasty


Percutaneous osteosynthesis


Compilance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    H. Chen, R.S. Sippel, M.S. O’Dorisio, A.I. Vinik, R.V. Lloyd, K. Pacak, and North American Neuroendocrine Tumor Society (NANETS), The North American Neuroendocrine Tumor Society consensus guideline for the diagnosis and management of neuroendocrine tumors: pheochromocytoma, paraganglioma, and medullary thyroid cancer. Pancreas 39, 775 (2010)CrossRefGoogle Scholar
  2. 2.
    L. Amar, M. Fassnacht, A.-P. Gimenez-Roqueplo, A. Januszewicz, A. Prejbisz, H. Timmers, P.-F. Plouin, Long-term postoperative follow-up in patients with apparently benign pheochromocytoma and paraganglioma. Horm. Metab. Res. 44, 385–9 (2012)CrossRefGoogle Scholar
  3. 3.
    G. Eisenhofer, S.R. Bornstein, F.M. Brouwers, N.-K.V. Cheung, P.L. Dahia, R.R. de Krijger, T.J. Giordano, L.A. Greene, D.S. Goldstein, H. Lehnert, W.M. Manger, J.M. Maris, H.P.H. Neumann, K. Pacak, B.L. Shulkin, D.I. Smith, A.S. Tischler, W.F. Young, Malignant pheochromocytoma: current status and initiatives for future progress. Endocr. Relat. Cancer 11, 423 (2004)CrossRefGoogle Scholar
  4. 4.
    L. Amar, E. Baudin, N. Burnichon, S. Peyrard, S. Silvera, J. Bertherat, X. Bertagna, M. Schlumberger, X. Jeunemaitre, A.-P. Gimenez-Roqueplo, P.-F. Plouin, Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. J. Clin. Endocrinol. Metab. 92, 3822 (2007)CrossRefGoogle Scholar
  5. 5.
    M. Ayala-Ramirez, J.L. Palmer, M.-C. Hofmann, M. de la Cruz, B.S. Moon, S.G. Waguespack, M.A. Habra, C. Jimenez, Bone metastases and skeletal-related events in patients with malignant pheochromocytoma and sympathetic paraganglioma. J. Clin. Endocrinol. Metab. 98, 1492 (2013)CrossRefGoogle Scholar
  6. 6.
    H.J.L.M. Timmers, C.C. Chen, J.A. Carrasquillo, M. Whatley, A. Ling, G. Eisenhofer, K.S. King, J.U. Rao, R.A. Wesley, K.T. Adams, K. Pacak, Staging and functional characterization of pheochromocytoma and paraganglioma by 18F-fluorodeoxyglucose (18F-FDG) positron emission tomography. J. Natl. Cancer Inst. 104, 700 (2012)CrossRefGoogle Scholar
  7. 7.
    S. Hescot, S. Leboulleux, L. Amar, D. Vezzosi, I. Borget, C. Bournaud-Salinas, C. de la Fouchardiere, R. Libé, C. Do Cao, P. Niccoli, A. Tabarin, I. Raingeard, C. Chougnet, S. Giraud, A.-P. Gimenez-Roqueplo, J. Young, F. Borson-Chazot, J. Bertherat, J.-L. Wemeau, X. Bertagna, P.-F. Plouin, M. Schlumberger, E. Baudin, and French group of Endocrine and Adrenal tumors (Groupe des Tumeurs Endocrines-REseau NAtional des Tumeurs ENdocrines and COrtico-MEdullo Tumeurs Endocrines networks), One-year progression-free survival of therapy-naive patients with malignant pheochromocytoma and paraganglioma. J. Clin. Endocrinol. Metab. 98, 4006 (2013)CrossRefGoogle Scholar
  8. 8.
    J.H. Lee, F. Barich, L.H. Karnell, R.A. Robinson, W.K. Zhen, B.J. Gantz, H.T. Hoffman, American College of Surgeons Commission on Cancer, and American Cancer Society, National Cancer Data Base report on malignant paragangliomas of the head and neck. Cancer 94, 730 (2002)CrossRefGoogle Scholar
  9. 9.
    F. Deschamps, G. Farouil, T. de Baere, Percutaneous ablation of bone tumors. Diagn. Interv. Imaging 95, 659 (2014)CrossRefGoogle Scholar
  10. 10.
    F. Deschamps, T. de Baere, A. Hakime, E. Pearson, G. Farouil, C. Teriitehau, L. Tselikas, Percutaneous osteosynthesis in the pelvis in cancer patients. Eur. Radiol. 26, 1631 (2016)CrossRefGoogle Scholar
  11. 11.
    F. Deschamps, T. de Baere, Cementoplasty of bone metastases. Diagn. Interv. Imaging 93, 685 (2012)CrossRefGoogle Scholar
  12. 12.
    F. Deschamps, G. Farouil, N. Ternes, A. Gaudin, A. Hakime, L. Tselikas, C. Teriitehau, E. Baudin, A. Auperin, T. de Baere, Thermal ablation techniques: a curative treatment of bone metastases in selected patients? Eur. Radiol. 24, 1971 (2014)CrossRefGoogle Scholar
  13. 13.
    U.S. Department of Health and Human Services. National Institutes of Health. (National Cancer Institute: Common Terminology Criteria for Adverse Events (CTCAE) Version 4. 03, 2010), Accessed 7 Sept 2017
  14. 14.
    Y. Kanda, Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 48, 452 (2013)CrossRefGoogle Scholar
  15. 15.
    K. Van Loon, L. Zhang, J. Keiser, C. Carrasco, K. Glass, M.-T. Ramirez, S. Bobiak, E.K. Nakakura, A.P. Venook, M.H. Shah, E.K. Bergsland, Bone metastases and skeletal-related events from neuroendocrine tumors. Endocr. Connect. 4, 9 (2015)CrossRefGoogle Scholar
  16. 16.
    M.O. Baerlocher, W.E. Saad, S. Dariushnia, J.D. Barr, J.K. McGraw, B. Nikolic; and Society of Interventional Radiology Standards of Practice Committee, Quality improvement guidelines for percutaneous vertebroplasty. J. Vasc. Interv. Radiol. 25, 165 (2014)CrossRefGoogle Scholar
  17. 17.
    A. Cotten, N. Boutry, B. Cortet, R. Assaker, X. Demondion, D. Leblond, P. Chastanet, B. Duquesnoy, H. Deramond, Percutaneous vertebroplasty: state of the art. Radiographics 18, 311 (1998)CrossRefGoogle Scholar
  18. 18.
    D.A. Palma, J.K. Salama, S.S. Lo, S. Senan, T. Treasure, R. Govindan, R. Weichselbaum, The oligometastatic state—separating truth from wishful thinking. Nat. Rev. Clin. Oncol. 11, 549 (2014)CrossRefGoogle Scholar
  19. 19.
    Z. Wang, D. Qiao, Y. Lu, D. Curtis, X. Wen, Y. Yao, H. Zhao, Systematic literature review and network meta-analysis comparing bone-targeted agents for the prevention of skeletal-related events in cancer patients with bone metastasis. Oncologist 20, 440 (2015)CrossRefGoogle Scholar
  20. 20.
    O. Sartor, R. Coleman, S. Nilsson, D. Heinrich, S.I. Helle, J.M. O’Sullivan, S.D. Fosså, A. Chodacki, P. Wiechno, J. Logue, A. Widmark, D.C. Johannessen, P. Hoskin, N.D. James, A. Solberg, I. Syndikus, N.J. Vogelzang, C.G. O’Bryan-Tear, M. Shan, Ø.S. Bruland, C. Parker, Effect of radium-223 dichloride on symptomatic skeletal events in patients with castration-resistant prostate cancer and bone metastases: results from a phase 3, double-blind, randomised trial. Lancet Oncol. 15, 738 (2014).CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Guillaume Gravel
    • 1
    Email author
  • Sophie Leboulleux
    • 2
  • Lambros Tselikas
    • 1
  • Flora Fassio
    • 2
  • Mohamed Berraf
    • 1
  • Amandine Berdelou
    • 2
  • Bakar Ba
    • 1
  • Segolene Hescot
    • 2
  • Julien Hadoux
    • 2
  • Martin Schlumberger
    • 2
  • Abir Al Ghuzlan
    • 3
  • France Nguyen
    • 4
  • Mathieu Faron
    • 5
  • Thierry de Baere
    • 1
  • Eric Baudin
    • 2
  • Frederic Deschamps
    • 1
  1. 1.Department of Interventional RadiologyGustave Roussy Cancer CenterVillejuifFrance
  2. 2.Department of Nuclear Medicine and Endocrine OncologyGustave Roussy Cancer CenterVillejuifFrance
  3. 3.Department of AnatomopathologyGustave Roussy Cancer CenterVillejuifFrance
  4. 4.Department of RadiotherapyGustave Roussy Cancer CenterVillejuifFrance
  5. 5.Department of SurgeryGustave Roussy Cancer CenterVillejuifFrance

Personalised recommendations