Analysis of factors influencing hungry bone syndrome in patients with secondary hyperparathyroidism after parathyroidectomy_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

HUANG Sheng ¹ , LIU Xiaofang ² , LIAO Xiwei ¹ , DENG Lin ¹ ,  ZHANG Zaizhong ¹

1. Department of General Surgery, The 900th Hospital of Joint Logistics Support Force, Fuzong Clinical Medical College of Fujian Medical University, Dongfang Hospital of Xiamen University, Fuzhou 350025, P. R. China;
2. Department of Thyroid and Breast Surgery, Mengchao Hepatobiliary Hospital of Fujian Medical University, Fuzhou 350025, P. R. China;

Corresponding author：

ZHANG Zaizhong, Email: fzptwk@126.com

Keywords：

secondary hyperparathyroidism; hungry bone syndrome; alkaline phosphatase

DOI：

10.7507/1007-9424.202305007

Video：

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Objective To analyze the factors influencing the hungry bone syndrome (HBS) in patients with secondary hyperparathyroidism (SHPT) after parathyroidectomy. Methods The clinical data of patients who underwent parathyroidectomy for SHPT in the 900th Hospital of the Joint Logistics Support Force from January 2016 to May 2021 were retrospectively analyzed. The risk factors for HBS were analyzed by binary logistic regression analysis. The cut-off value of risk factors for predicting postoperative HBS was analyzed by using recieve operating characteristic (ROC) curve. Results A total of 89 patients were included in this study, including 44 males and 45 females, with (47±11) years old. There were 42 (47.2%) patients with HBS. Compared with the patients without HBS, the patients with HBS was younger and had higher levels of preoperative parathyroid hormone, potassium, and alkaline phosphatase (ALP), the differences were statistically different (P<0.05). The multivariate binary logistic regression analysis showed that the higher preoperative ALP level was a risk factor for the HBS [OR (95%CI) = 1.014 (1.007, 1.020), P<0.001]. The area under the ROC curve (95%CI) of the preoperative ALP level in distinguishing the patients with HBS from without HBS was 0.957 (0.919, 0.996), and the optimal cut-off value of ALP for predicting postoperative HBS was 278.90 U/L. Conclusions From the preliminary results of this study, it can be concluded that bone conversion status can be differentiated according to preoperative ALP level in patients with SHPT. When preoperative ALP level is higher than cut-off value, it is recommended that calcium supplementation should be given as soon as possible and blood calcium level should be closely monitored.

Citation： HUANG Sheng, LIU Xiaofang, LIAO Xiwei, DENG Lin, ZHANG Zaizhong. Analysis of factors influencing hungry bone syndrome in patients with secondary hyperparathyroidism after parathyroidectomy. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(8): 926-930. doi: 10.7507/1007-9424.202305007 Copy

1.	Bonjour JP, Kohrt W, Levasseur R, et al. Biochemical markers for assessment of calcium economy and bone metabolism: application in clinical trials from pharmaceutical agents to nutritional products. Nutr Res Rev, 2014, 27(2): 252-267.
2.	吴承倢, 卢春燕. 术后骨饥饿综合征. 中国普外基础与临床杂志, 2021, 28(2): 265-270.
3.	Silva BC, Bilezikian JP. Parathyroid hormone: anabolic and catabolic actions on the skeleton. Curr Opin Pharmacol, 2015, 22: 41-50.
4.	Williams-Karnesky RL, Krumeich L, Wachtel H, et al. Data to inform counseling on parathyroidectomy for secondary hyperparathyroidism of renal origin. Surgery, 2022, 171(1): 63-68.
5.	中国医师协会外科医师分会甲状腺外科医师委员会, 中国研究型医院学会甲状腺疾病专业委员会. 慢性肾功能衰竭继发甲状旁腺功能亢进外科临床实践专家共识. 中国实用外科杂志, 2016, 36(5): 481-486.
6.	中国医师协会外科医师分会甲状腺外科医师委员会, 中国研究型医院学会甲状腺疾病专业委员会. 慢性肾脏病继发甲状旁腺功能亢进外科临床实践中国专家共识(2021版). 中国实用外科杂志, 2021, 41(8): 841-848.
7.	Witteveen JE, van Thiel S, Romijn JA, et al. Hungry bone syndrome: still a challenge in the post-operative management of primary hyperparathyroidism: a systematic review of the literature. Eur J Endocrinol, 2013, 168(3): R45-R53. doi: 10.1530/EJE-12-0528.
8.	Cartwright C, Anastasopoulou C. Hungry bone syndrome. StatPearls. Treasure Island (FL), 2021.
9.	Cartwright C, Anastasopoulou C. Hungry bone syndrome. StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing, 2022.
10.	张凌, 闫彩芸. 难治性继发性甲状旁腺功能亢进症治疗时机选择. 中国实用内科杂志, 2013, 33(2): 131-133.
11.	Rodríguez-Ortiz ME, Pendón-Ruiz de Mier MV, Rodríguez M. Parathyroidectomy in dialysis patients: indications, methods, and consequences. Semin Dial, 2019, 32(5): 444-451.
12.	安宏, 庞毅, 徐辉, 等. 慢性肾脏病继发甲状旁腺功能亢进的手术治疗. 天津医药, 2018, 46(12): 1357-1362.
13.	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 (2011), 2017, 7(1): 1-59.
14.	Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Work Group. KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of Chronic Kidney Disease-Mineral and Bone Disorder (CKD-MBD). Kidney Int Suppl, 2009, (113): S1-S130.
15.	Kidney Disease Outcomes Quality Initiative (K/DOQI) Group. K/DOQI clinical practice guidelines for management of dyslipidemias in patients with kidney disease. Am J Kidney Dis, 2003, 41(4 Suppl 3): Ⅰ-Ⅳ, S1-S91.
16.	Albright F. A page out of the history of hyperparathyroidism. J Clin Endocrinol Metab, 1948, 8(8): 637-657.
17.	Yang M, Zhang L, Huang L, et al. Factors predictive of critical value of hypocalcemia after total parathyroidectomy without autotransplantation in patients with secondary hyperparathyroidism. Ren Fail, 2016, 38(8): 1224-1227.
18.	Tsai WC, Peng YS, Chiu YL, et al. Risk factors for severe hypocalcemia after parathyroidectomy in prevalent dialysis patients with secondary hyperparathyroidism. Int Urol Nephrol, 2015, 47(7): 1203-1207.
19.	赵沙沙, 闻萍, 甘巍, 等. 甲状旁腺全切术患者术后严重低钙血症危险因素分析. 中华肾脏病杂志, 2019, 35(7): 494-498.
20.	Ko WC, Liu CL, Lee JJ, et al. Osteocalcin is an independent predictor for hungry bone syndrome after parathyroidectomy. World J Surg, 2020, 44(3): 795-802.
21.	段文浩, 晏影, 时潇诺, 等. 维持性透析患者甲状旁腺切除术后严重骨饥饿综合征预测因素分析. 河南外科学杂志, 2023, 29(1): 42-46.
22.	王佳莹, 谭峰, 吴宸极, 等. 维持性血液透析伴继发性甲状旁腺功能亢进患者甲状旁腺切除术后骨饥饿综合征发生影响因素及血清离子变化特征. 陕西医学杂志, 2021, 50(3): 334-337.
23.	Kritmetapak K, Kongpetch S, Chotmongkol W, et al. Incidence of and risk factors for post-parathyroidectomy hungry bone syndrome in patients with secondary hyperparathyroidism. Ren Fail, 2020, 42(1): 1118-1126.
24.	Ge Y, Yang G, Wang N, et al. Bone metabolism markers and hungry bone syndrome after parathyroidectomy in dialysis patients with secondary hyperparathyroidism. Int Urol Nephrol, 2019, 51(8): 1443-1449.
25.	Ishani A, Liu J, Wetmore JB, et al. Clinical outcomes after parathyroidectomy in a nationwide cohort of patients on hemodialysis. Clin J Am Soc Nephrol, 2015, 10(1): 90-97.
26.	Goh BL, Yudisthra MG, Hisham AN. Alkaline phosphatase predicts calcium requirements after total parathyroidectomy in patients receiving dialysis. Br J Surg, 2010, 97(2): 185-188.
27.	Cozzolino M, Gallieni M, Corsi C, et al. Management of calcium refilling post-parathyroidectomy in end-stage renal disease. J Nephrol, 2004, 17(1): 3-8.
28.	Loke SC, Kanesvaran R, Yahya R, et al. Efficacy of an intravenous calcium gluconate infusion in controlling serum calcium after parathyroidectomy for secondary hyperparathyroidism. Ann Acad Med Singap, 2009, 38(12): 1074-1080.
29.	Tan JH, Tan HC, Loke SC, et al. Novel calcium infusion regimen after parathyroidectomy for renal hyperparathyroidism. Nephrology (Carlton), 2017, 22(4): 308-315.
30.	Wong J, Fu WH, Lim ELA, et al. Hungry bone syndrome after parathyroidectomy in end-stage renal disease patients: review of an alkaline phosphatase-based treatment protocol. Int Urol Nephrol, 2020, 52(3): 557-564.

1. Bonjour JP, Kohrt W, Levasseur R, et al. Biochemical markers for assessment of calcium economy and bone metabolism: application in clinical trials from pharmaceutical agents to nutritional products. Nutr Res Rev, 2014, 27(2): 252-267.
2. 吴承倢, 卢春燕. 术后骨饥饿综合征. 中国普外基础与临床杂志, 2021, 28(2): 265-270.
3. Silva BC, Bilezikian JP. Parathyroid hormone: anabolic and catabolic actions on the skeleton. Curr Opin Pharmacol, 2015, 22: 41-50.
4. Williams-Karnesky RL, Krumeich L, Wachtel H, et al. Data to inform counseling on parathyroidectomy for secondary hyperparathyroidism of renal origin. Surgery, 2022, 171(1): 63-68.
5. 中国医师协会外科医师分会甲状腺外科医师委员会, 中国研究型医院学会甲状腺疾病专业委员会. 慢性肾功能衰竭继发甲状旁腺功能亢进外科临床实践专家共识. 中国实用外科杂志, 2016, 36(5): 481-486.
6. 中国医师协会外科医师分会甲状腺外科医师委员会, 中国研究型医院学会甲状腺疾病专业委员会. 慢性肾脏病继发甲状旁腺功能亢进外科临床实践中国专家共识(2021版). 中国实用外科杂志, 2021, 41(8): 841-848.
7. Witteveen JE, van Thiel S, Romijn JA, et al. Hungry bone syndrome: still a challenge in the post-operative management of primary hyperparathyroidism: a systematic review of the literature. Eur J Endocrinol, 2013, 168(3): R45-R53. doi: 10.1530/EJE-12-0528.
8. Cartwright C, Anastasopoulou C. Hungry bone syndrome. StatPearls. Treasure Island (FL), 2021.
9. Cartwright C, Anastasopoulou C. Hungry bone syndrome. StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing, 2022.
10. 张凌, 闫彩芸. 难治性继发性甲状旁腺功能亢进症治疗时机选择. 中国实用内科杂志, 2013, 33(2): 131-133.
11. Rodríguez-Ortiz ME, Pendón-Ruiz de Mier MV, Rodríguez M. Parathyroidectomy in dialysis patients: indications, methods, and consequences. Semin Dial, 2019, 32(5): 444-451.
12. 安宏, 庞毅, 徐辉, 等. 慢性肾脏病继发甲状旁腺功能亢进的手术治疗. 天津医药, 2018, 46(12): 1357-1362.
13. 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 (2011), 2017, 7(1): 1-59.
14. Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Work Group. KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of Chronic Kidney Disease-Mineral and Bone Disorder (CKD-MBD). Kidney Int Suppl, 2009, (113): S1-S130.
15. Kidney Disease Outcomes Quality Initiative (K/DOQI) Group. K/DOQI clinical practice guidelines for management of dyslipidemias in patients with kidney disease. Am J Kidney Dis, 2003, 41(4 Suppl 3): Ⅰ-Ⅳ, S1-S91.
16. Albright F. A page out of the history of hyperparathyroidism. J Clin Endocrinol Metab, 1948, 8(8): 637-657.
17. Yang M, Zhang L, Huang L, et al. Factors predictive of critical value of hypocalcemia after total parathyroidectomy without autotransplantation in patients with secondary hyperparathyroidism. Ren Fail, 2016, 38(8): 1224-1227.
18. Tsai WC, Peng YS, Chiu YL, et al. Risk factors for severe hypocalcemia after parathyroidectomy in prevalent dialysis patients with secondary hyperparathyroidism. Int Urol Nephrol, 2015, 47(7): 1203-1207.
19. 赵沙沙, 闻萍, 甘巍, 等. 甲状旁腺全切术患者术后严重低钙血症危险因素分析. 中华肾脏病杂志, 2019, 35(7): 494-498.
20. Ko WC, Liu CL, Lee JJ, et al. Osteocalcin is an independent predictor for hungry bone syndrome after parathyroidectomy. World J Surg, 2020, 44(3): 795-802.
21. 段文浩, 晏影, 时潇诺, 等. 维持性透析患者甲状旁腺切除术后严重骨饥饿综合征预测因素分析. 河南外科学杂志, 2023, 29(1): 42-46.
22. 王佳莹, 谭峰, 吴宸极, 等. 维持性血液透析伴继发性甲状旁腺功能亢进患者甲状旁腺切除术后骨饥饿综合征发生影响因素及血清离子变化特征. 陕西医学杂志, 2021, 50(3): 334-337.
23. Kritmetapak K, Kongpetch S, Chotmongkol W, et al. Incidence of and risk factors for post-parathyroidectomy hungry bone syndrome in patients with secondary hyperparathyroidism. Ren Fail, 2020, 42(1): 1118-1126.
24. Ge Y, Yang G, Wang N, et al. Bone metabolism markers and hungry bone syndrome after parathyroidectomy in dialysis patients with secondary hyperparathyroidism. Int Urol Nephrol, 2019, 51(8): 1443-1449.
25. Ishani A, Liu J, Wetmore JB, et al. Clinical outcomes after parathyroidectomy in a nationwide cohort of patients on hemodialysis. Clin J Am Soc Nephrol, 2015, 10(1): 90-97.
26. Goh BL, Yudisthra MG, Hisham AN. Alkaline phosphatase predicts calcium requirements after total parathyroidectomy in patients receiving dialysis. Br J Surg, 2010, 97(2): 185-188.
27. Cozzolino M, Gallieni M, Corsi C, et al. Management of calcium refilling post-parathyroidectomy in end-stage renal disease. J Nephrol, 2004, 17(1): 3-8.
28. Loke SC, Kanesvaran R, Yahya R, et al. Efficacy of an intravenous calcium gluconate infusion in controlling serum calcium after parathyroidectomy for secondary hyperparathyroidism. Ann Acad Med Singap, 2009, 38(12): 1074-1080.
29. Tan JH, Tan HC, Loke SC, et al. Novel calcium infusion regimen after parathyroidectomy for renal hyperparathyroidism. Nephrology (Carlton), 2017, 22(4): 308-315.
30. Wong J, Fu WH, Lim ELA, et al. Hungry bone syndrome after parathyroidectomy in end-stage renal disease patients: review of an alkaline phosphatase-based treatment protocol. Int Urol Nephrol, 2020, 52(3): 557-564.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Analysis of factors influencing hungry bone syndrome in patients with secondary hyperparathyroidism after parathyroidectomy

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