Abstract
Background
Reoperation for recurrent or persistent secondary hyperparathyroidism (SHPT) after parathyroidectomy is challenging due to surgical scars and postoperative adhesions. Therefore, there is an increasing need to develop a new minimally invasive therapy.
Objective
To analyze the efficacy of ultrasound (US)-guided radiofrequency ablation (RFA) in patients with recurrent or persistent SHPT after parathyroidectomy.
Patients and methods
From March 2013 to January 2022, 20 enlarged parathyroid glands in 10 patients with recurrent or persistent SHPT were treated with US-guided RFA. The levels of serum intact parathyroid hormone (iPTH), calcium (Ca), phosphorus (P), and alkaline phosphatase (ALP), as well as clinical symptoms, were compared before and after RFA. The ablation procedure-related complications were also evaluated. The target range for iPTH levels was approximately 2–9 times the upper limit of normal (130–585 pg/mL).
Results
The mean follow-up time was 49.6 ± 34.5 months (range from 6 to101 months). The levels of serum iPTH, Ca, and P decreased significantly one day post-ablation. Six months after RFA, 70% of patients reached the targets for iPTH, and 50% of patients reached targets at the end of follow-up. Two patients underwent repeat ablation at 9 months and 6 years after RFA, respectively, due to persistently elevated iPTH levels, and both had serum iPTH concentrations in the recommended range at the recent follow-up visit. The patients’ clinical symptoms significantly improved after ablation. Major complications after RFA included hoarseness (2/10) and permanent hypoparathyroidism (1/10). Severe hypocalcemia occurred in four patients (4/10) after ablation.
Conclusion:
US-guided percutaneous RFA for recurrent or persistent SHPT is safe, efficacious, and repeatable, and can significantly improve hyperparathyroidism-related symptoms.
Similar content being viewed by others
References
W.L. Lau, Y. Obi, K. Kalantar-Zadeh, Parathyroidectomy in the management of secondary hyperparathyroidism. Clin. J. Am. Soc. Nephrol. 13(6), 952–961 (2018)
J.B. Cannata-Andía, J.L. Fernández-Martín, C. Zoccali, G.M. London, F. Locatelli, M. Ketteler, A. Ferreira, A. Covic, J. Floege, J.L. Górriz et al. Current management of secondary hyperparathyroidism: a multicenter observational study (COSMOS). J. Nephrol. 21(3), 290–298 (2008)
X. Kong, L. Zhang, L. Zhang, N. Chen, Y. Gu, X. Yu, W. Liu, J. Chen, L. Peng, W. Yuan et al. Mineral and bone disorder in Chinese dialysis patients: a multicenter study. BMC Nephrol. 13, 116 (2012)
E. Zitt, M. Rix, P. Ureña Torres, D. Fouque, S.H. Jacobson, F. Pétavy, B. Dehmel, M. Ryba, Effectiveness of cinacalcet in patients with recurrent/persistent secondary hyperparathyroidism following parathyroidectomy: results of the ECHO study. Nephrol. Dial. Transpl. 26(6), 1956–1961 (2011)
R. Schneider, E.P. Slater, E. Karakas, D.K. Bartsch, K. Schlosser, Initial parathyroid surgery in 606 patients with renal hyperparathyroidism. World J. Surg. 36(2), 318–326 (2012)
W.J. Johnson, J.T. McCarthy, J.A. van Heerden, S. Sterioff, C.S. Grant, P.C. Kao, Results of subtotal parathyroidectomy in hemodialysis patients. Am. J. Med. 84(1), 23–32 (1988)
E.R. Gagné, P. Ureña, S. Leite-Silva, J. Zingraff, A. Chevalier, E. Sarfati, C. Dubost, T.B. Drüeke, Short- and long-term efficacy of total parathyroidectomy with immediate autografting compared with subtotal parathyroidectomy in hemodialysis patients. J. Am. Soc. Nephrology: JASN, 3(4), 1008–1017 (1992)
G. Gasparri, M. Camandona, G.C. Abbona, M. Papotti, A. Jeantet, E. Radice, B. Mullineris, M. Dei Poli, Secondary and tertiary hyperparathyroidism: causes of recurrent disease after 446 parathyroidectomies. Ann. Surg. 233(1), 65–69 (2001)
A. Simental, R.L. Ferris, Reoperative parathyroidectomy. Otolaryngolog. Clin. North Am. 41(6), 1269–1274 (2008)
L. Yan, X. Li, Y. Li, J. Xiao, M. Zhang, Y. Luo, Comparison of ultrasound-guided radiofrequency ablation versus thyroid lobectomy for T1bN0M0 papillary thyroid carcinoma. Eur. Radio. 33(1), 730–740 (2023)
F. Izzo, V. Granata, R. Grassi, R. Fusco, R. Palaia, P. Delrio, G. Carrafiello, D. Azoulay, A. Petrillo, S.A. Curley, Radiofrequency ablation and microwave ablation in liver tumors: an update. Oncologist 24(10), e990–e1005 (2019)
F.G. Pareja, P.P. Naranjo, M.D.R. Olmedilla, A.C. Pena, Radiofrequency ablation for thyroid and parathyroid disease. Radiologia 64(4), 383–392 (2022)
Y. Wei, C.-Z. Peng, S.-R. Wang, J.-F. He, L.-L. Peng, Z.-L. Zhao, X.-J. Cao, Y. Li, M.-A. Yu, Effectiveness and safety of thermal ablation in the treatment of primary hyperparathyroidism: a multicenter study. J. Clin. Endocrinol. Metab. 106(9), 2707–2717 (2021)
F.Y. Liu, Y. Liu, C.Z. Peng, M.G. Yu, S.S. Wu, L.X. Qian, Z.Y. Han, J. Yu, H.H. Chai, P. Liang, Ultrasound-guided microwave and radiofrequency ablation for primary hyperparathyroidism: a prospective, multicenter study. Eur. Radiol. 32(11), 7743–7754 (2022)
M. Ren, D. Zheng, J. Wu, Y. Liu, C. Peng, W. Shen, B. Lin, Efficacy and safety of radiofrequency ablation versus parathyroidectomy for secondary hyperparathyroidism in dialysis patients: a single-center retrospective study. Sci. Rep. 12(1), 10289 (2022)
C.C. Chen, H.L. Chen, P.L. Chiang, S.D. Luo, Y.H. Chang, W.C. Chen, C.K. Wang, A.N. Lin, Y.S. Chen, S.Y. Chi et al. Efficacy and safety of radiofrequency ablation for primary and secondary hyperparathyroidism with or without previous parathyroidectomy: a retrospective study. Int. J. Hyperth. : Off. J. Eur. Soc. Hyperther. Oncol., North Am. Hyperth. Group 39(1), 907–917 (2022)
M.-A. Yu, L. Yao, L. Zhang, L. Peng, L. Zhuo, Y. Zhang, W. Li, M.-D. Lv, Safety and efficiency of microwave ablation for recurrent and persistent secondary hyperparathyroidism after parathyroidectomy: a retrospective pilot study. Int. J. Hyperth. 32(2), 180–186 (2016)
H.H. Chen, C.J. Lin, C.J. Wu, C.T. Lai, J. Lin, S.P. Cheng, T.L. Yang, Chemical ablation of recurrent and persistent secondary hyperparathyroidism after subtotal parathyroidectomy. Ann. Surg. 253(4), 786–790 (2011)
L. Zhuo, L.L. Peng, Y.M. Zhang, Z.H. Xu, G.M. Zou, X. Wang, W.G. Li, M.D. Lu, M.A. Yu, US-guided microwave ablation of hyperplastic parathyroid glands: safety and efficacy in patients with end-stage renal disease-a pilot study. Radiology 282(2), 576–584 (2017)
Erratum: Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Update Work Group, KDIGO 2017 clinical practice guideline update for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int. Suppl. Kidney Int. Suppl. 7(1), 1–59 (2017)
D. Sacks, T.E. McClenny, J.F. Cardella, C.A. Lewis, Society of interventional radiology clinical practice guidelines. J. Vasc. Inter. Radio. 14(9 Pt 2), S199–202 (2003)
C. Kim, J.H. Lee, Y.J. Choi, W.B. Kim, T.Y. Sung, J.H. Baek, Complications encountered in ultrasonography-guided radiofrequency ablation of benign thyroid nodules and recurrent thyroid cancers. Eur. Radio. 27(8), 3128–3137 (2017)
Z. Zeng, C.Z. Peng, J.B. Liu, Y.W. Li, H.F. He, Q.H. Hu, B. Lin, X.G. Shen, Efficacy of ultrasound-guided radiofrequency ablation of parathyroid hyperplasia: single session vs. two-session for effect on hypocalcemia. Sci. Rep. 10(1), 6206 (2020)
H.R. Choi, M.A. Aboueisha, A.S. Attia, M. Omar, E.L. A, E.A. Toraih, M. Shama, W.Y. Chung, J.J. Jeong, E. Kandil, Outcomes of subtotal parathyroidectomy versus total parathyroidectomy with autotransplantation for tertiary hyperparathyroidism: multi-institutional study. Ann. Surg. 274(4), 674–679 (2021)
H.I. Lu, F.F. Chou, S.Y. Chi, S.C. Huang, Thoracoscopic removal of hypertrophic mediastinal parathyroid glands in recurrent secondary hyperparathyroidism. World J. Surg. 39(2), 400–409 (2015)
L. Zhu, F. Cheng, X. Zhu, B. Zhou, Y. Xu, Y. Wu, C. Shao, Safety and effectiveness of reoperation for persistent or recurrent drug refractory secondary hyperparathyroidism. Gland Surg. 9(2), 401–408 (2020)
L. Alvarado, N. Sharma, R. Lerma, A. Dwivedi, A. Ahmad, A. Hechanova, F. Payan-Schober, A. Nwosu, E. Alkhalili, Parathyroidectomy versus cinacalcet for the treatment of secondary hyperparathyroidism in hemodialysis patients. World J. Surg. 46(4), 813–819 (2022)
S. Yumita, Intervention for recurrent secondary hyperparathyroidism from a residual parathyroid gland. Nephrol. Dial. Transpl. 18, iii62–64 (2003)
R. Eriguchi, J. Umakoshi, Y. Tominaga, Y. Sato, Successful treatment of inoperable recurrent secondary hyperparathyroidism with cinacalcet HCl. NDT 1(4), 218–220 (2008)
W.G. Douthat, G. Cardozo, G. Garay, S. Orozco, C. Chiurchiu, J. de la Fuente, J. de Arteaga, P.U. Massari, Use of percutaneous ethanol injection therapy for recurrent secondary hyperparathyroidism after subtotal parathyroidectomy. Int J. Nephrol. 2011, 246734 (2011)
G.M. Chertow, G.A. Block, R. Correa-Rotter, T.B. Drüeke, J. Floege, W.G. Goodman, C.A. Herzog, Y. Kubo, G.M. London, K.W. Mahaffey et al. Effect of cinacalcet on cardiovascular disease in patients undergoing dialysis. N. Engl. J. Med. 367(26), 2482–2494 (2012)
E. Zitt, M. Rix, P. Urena Torres, D. Fouque, S.H. Jacobson, F. Petavy, B. Dehmel, M. Ryba, Effectiveness of cinacalcet in patients with recurrent/persistent secondary hyperparathyroidism following parathyroidectomy: results of the ECHO study. Nephrol. Dial. Transpl. 26(6), 1956–1961 (2011)
R. Kovatcheva, J. Vlahov, J. Stoinov, F. Lacoste, C. Ortuno, K. Zaletel, US-guided high-intensity focused ultrasound as a promising non-invasive method for treatment of primary hyperparathyroidism. Eur. Radio. 24(9), 2052–2058 (2014)
N. Singh Ospina, G.B. Thompson, R.A. Lee, C.C. Reading, W.F. Young Jr, Safety and efficacy of percutaneous parathyroid ethanol ablation in patients with recurrent primary hyperparathyroidism and multiple endocrine neoplasia type 1. J. Clin. Endocrinol. Metab. 100(1), E87–90 (2015)
P. Li Zhuo, M. Li-li Peng, P. Yu-mei Zhang, M. Zhi-hong Xu, M. Gu-ming Zou, M. Xin Wang, P. Wen-ge Li, P. Ming-de Lu, P. Ming-an Yu, Us-guided Microwave ablation of hyperplastic parathyroid glands: safety and efficacy in patients with end-stage renal disease—a pilot study. Radiology 282(2), 576–584 (2016)
F. Koiwa, T. Kakuta, R. Tanaka, S. Yumita, Efficacy of percutaneous ethanol injection therapy (PEIT) is related to the number of parathyroid glands in haemodialysis patients with secondary hyperparathyroidism. Nephrol., Dialysis, Transplant. : Off. Publ. Eur. Dialysis Transpl. Assoc. - Eur. Ren. Assoc. 22(2), 522–528 (2007)
M.A. Yu, L. Yao, L. Zhang, L. Peng, L. Zhuo, Y. Zhang, W. Li, M.D. Lv, Safety and efficiency of microwave ablation for recurrent and persistent secondary hyperparathyroidism after parathyroidectomy: a retrospective pilot study. Int. J. Hyperth. : Off. J. Eur. Soc. Hyperth. Oncol., North Am. Hyperth. Group 32(2), 180–186 (2016)
L. Appelbaum, S.N. Goldberg, T. Ierace, G. Mauri, L. Solbiati, US-guided laser treatment of parathyroid adenomas. Int. J. Hyperth. : Off. J. Eur. Soc. Hyperth. Oncol., North Am. Hyperth. Group 37(1), 366–372 (2020)
G. Adda, A. Scillitani, P. Epaminonda, S. Di Lembo, F. Motta, P. Cecconi, G. Vecchi, M. Arosio, I. Chiodini, Ultrasound-guided laser thermal ablation for parathyroid adenomas: analysis of three cases with a three-year follow-up. Horm. Res. 65(5), 231–234 (2006)
N.E. Cusano, J.A. Lee, R.F. Wetmore, E. Kazam, J.P. Bilezikian, Primary hyperparathyroidism after laser therapy to the larynx. Endocr. Pr. 19(5), 888–890 (2013)
C.E. Ambrosini, L. Cianferotti, A. Picone, L. Torregrossa, G. Segnini, G. Frustaci, F. Cetani, F. Basolo, C. Marcocci, P. Miccoli, High-intensity focused ultrasound as an alternative to the surgical approach in primary hyperparathyroidism: a preliminary experience. J. Endocrinol. Investig. 34(9), 655–659 (2011)
R.D. Kovatcheva, J.D. Vlahov, J.I. Stoinov, G.G. Kirilov, S.G. Krivoshiev, F. Arnaud, C. Ortuno, T.B. Drüeke, High-intensity focussed ultrasound (HIFU) treatment in uraemic secondary hyperparathyroidism. Nephrol., Dialysis, Transplant. : Off. Publ. Eur. Dialysis Transpl. Assoc. - Eur. Ren. Assoc. 27(1), 76–80 (2012)
L. Zhuo, L. Zhang, L.L. Peng, Y. Yang, H.T. Lu, D.P. Chen, W.G. Li, M.A. Yu, Microwave ablation of hyperplastic parathyroid glands is a treatment option for end-stage renal disease patients ineligible for surgical resection. Int. J. Hyperth. : Off. J. Eur. Soc. Hyperthermic Oncol., North Am. Hyperth. Group 36(1), 29–35 (2019)
G. Wang, S. Liu, X. Liu, L. Qian, Z. Diao, W. Liu, Microwave ablation: an effective treatment for mild-to-moderate secondary hyperparathyroidism in patients undergoing haemodialysis. Int J. Hyperthermia: 33(8), 946–952 (2017)
I. Nawrot, W. Chudzinski, T. Ciacka, M. Barczynski, J. Szmidt, Reoperations for persistent or recurrent primary hyperparathyroidism: results of a retrospective cohort study at a tertiary referral center. Med Sci. Monit. 20, 1604–1612 (2014)
W. Ni, Y. Yuan, X. Chu, G. Chen, X. Han, J. Li, X. Wu, J. Wang, C. Liu, S. Xu, Bone turnover markers in response to ultrasound-guided microwave ablation for primary hyperparathyroidism. Front. Endocrinol. 12, 782050 (2021)
Y. Wei, C.Z. Peng, S.R. Wang, J.F. He, L.L. Peng, Z.L. Zhao, X.J. Cao, Y. Li, M.A. Yu, Effectiveness and safety of thermal ablation in the treatment of primary hyperparathyroidism: a multicenter study. J. Clin. Endocrinol. Metab. 106(9), 2707–2717 (2021)
S.J. Bo, X.F. Xu, C.Y. Qiu, T.T. Wang, Y.D. Ning, H.Y. Li, Re-operation treatment in uremic patients complicated with persistent secondary hyperparathyroidism after parathyroidectomy with autotransplantation. Lin. Chuang Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 32(2), 142–147 (2018)
Funding
The study was supported by National Natural Science Foundation of China (Grant No: 81901754). The authors are very grateful to the foundation for its support.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Tingting Jiang, Erya Deng and Huihui Chai. The first draft of the manuscript was written by Tingting Jiang and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethics approval
This study was approved by the Human Ethics Committee of the enrolled institutes.
Consent to participate
Written informed consent was obtained from all patients prior to ablation. And the need for individual informed consent was waived because of the retrospective nature of the study.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Jiang, T., Deng, E., Chai, H. et al. Radiofrequency ablation for patients with recurrent or persistent secondary hyperparathyroidism after parathyroidectomy: initial experience. Endocrine 83, 681–690 (2024). https://doi.org/10.1007/s12020-023-03513-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12020-023-03513-5