Postoperative hungry bone syndrome_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

WU Chengjie ,  LU Chunyan

Department of Endocrinology and Metabolism/Parathyroid MDT Diagnosis and Treatment Team, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

LU Chunyan, Email: lcyan8306@163.com

Keywords：

hungry bone syndrome; hyperparathyroidism; treatment; review

DOI：

10.7507/1007-9424.202009114

Video：

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Objective To summarize the mechanism, risk factors, clinical manifestations, and medical treatment of hungry bone syndrome (HBS) in patients with hyperparathyroidism after parathyroidectomy, and to provide clinicians with reference for disease diagnosis and treatment.Method The related literatures about HBS in patients were collected and reviewed with clinical experience.Results HBS was a group of clinical syndromes mainly manifested as hypocalcemia after parathyroidectomy in patients with high bone turnover state before operation, with a high incidence, and the main purpose of treatment was achieved by supplementing calcium and vitamin D.Conclusions HBS requires reasonable diagnosis and timely treatment by clinicians. Patients can achieve long-term blood calcium and phosphorus stability and bone mass growth through medical treatment.

Citation： WU Chengjie, LU Chunyan. Postoperative hungry bone syndrome. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(2): 265-270. doi: 10.7507/1007-9424.202009114 Copy

1.	Albright F, Reifenstein EC Jr. The Parathyroid glands and metabolic bone disease. Gastroenterology, 1950, 14(4): 594-595.
2.	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.
3.	Chen P, Satterwhite JH, Licata AA, et al. Early changes in biochemical markers of bone formation predict BMD response to teriparatide in postmenopausal women with osteoporosis. J Bone Miner Res, 2005, 20(6): 962-970.
4.	Silva BC, Bilezikian JP. Parathyroid hormone: anabolic and catabolic actions on the skeleton. Curr Opin Pharmacol, 2015, 22: 41-50.
5.	Ma YL, Cain RL, Halladay DL, et al. Catabolic effects of continuous human PTH (1-38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation. Endocrinology, 2001, 142(9): 4047-4054.
6.	Liu S, Zhu W, Li S, et al. The effect of bovine parathyroid hormone withdrawal on MC3T3-E1 cell proliferation and phosphorus metabolism. PLoS One, 2015, 10(3): e0120402.
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.
8.	Jain N, Reilly RF. Hungry bone syndrome. Curr Opin Nephrol Hypertens, 2017, 26(4): 250-255.
9.	Jakubauskas M, Beiša V, Strupas K. Risk factors of developing the hungry bone syndrome after parathyroidectomy for primary hyperparathyroidism. Acta Med Litu, 2018, 25(1): 45-51.
10.	Goldfarb M, Gondek SS, Lim SM, et al. Postoperative hungry bone syndrome in patients with secondary hyperparathyroidism of renal origin. World J Surg, 2012, 36(6): 1314-1319.
11.	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.
12.	Brasier AR, Nussbaum SR. Hungry bone syndrome: clinical and biochemical predictors of its occurrence after parathyroid surgery. Am J Med, 1988, 84(4): 654-660.
13.	Guillén Martínez AJ, Smilg Nicolás C, Moraleda Deleito J, et al. Risk factors and evolution of calcium and parathyroid hormone levels in hungry bone syndrome after parthyroidectomy for primary hyperparathyroidism. Endocrinol Diabetes Nutr, 2020, 67(5): 310-316.
14.	Yang G, Zha X, Mao H, et al. Hypocalcemia-based prediction of hungry bone syndrome after parathyroidectomy in hemodialysis patients with refractory secondary hyperparathyroidism. J Int Med Res, 2018, 46(12): 4985-4994.
15.	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.
16.	Ho LY, Wong PN, Sin HK, et al. Risk factors and clinical course of hungry bone syndrome after total parathyroidectomy in dialysis patients with secondary hyperparathyroidism. BMC Nephrol, 2017, 18(1): 12.
17.	Wang M, Chen B, Zou X, et al. A Nomogram to predict hungry bone syndrome after parathyroidectomy in patients with secondary hyperparathyroidism. J Surg Res, 2020, 255: 33-41.
18.	Karunakaran P, Maharajan C, Ramalingam S, et al. Is hungry bone syndrome a cause of postoperative hypocalcemia after total thyroidectomy in thyrotoxicosis? A prospective study with bone mineral density correlation. Surgery, 2018, 163(2): 367-372.
19.	See AC, Soo KC. Hypocalcaemia following thyroidectomy for thyrotoxicosis. Br J Surg, 1997, 84(1): 95-97.
20.	Garla VV, Salim S, Kovvuru KR, et al. Hungry bone syndrome secondary to prostate cancer successfully treated with radium therapy. BMJ Case Rep, 2018, 2018: bcr2018225039.
21.	Sakai K, Tomoda Y, Saito H, et al. Hungry bone syndrome and osteoblastic bone metastasis from gastric cancer. QJM, 2020, hcaa125. [Online ahead of print].
22.	Isk Y, Goktas U, Yuzkat N, et al. Hungry bone syndrome as a cause of recurrent laryngospasm after parathyroidectomy. Eur J Anaesthesiol, 2011, 28(2): 142-143.
23.	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.
24.	Turner J, Gittoes N, Selby P. Society for Endocrinology Clinical Committee. Society for Endocrinology Endocrine Emergency Guidance: Emergency management of acute hypocalcaemia in adult patients. Endocr Connect, 2016, 5(5): G7-G8.
25.	卢春燕, 李志辉, 朱精强, 等. 术后甲状旁腺机能减退症的诊断及处理. 中国普外基础与临床杂志, 2014, 21(4): 501-506.
26.	Ureña P, Basile C, Grateau G, et al. Short-term effects of parathyroidectomy on plasma biochemistry in chronic uremia. Kidney Int, 1989, 36(1): 120-126.
27.	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.
28.	Nakagawa M, Emoto A, Nasu N, et al. Calcium supplement necessary to correct hypocalcemia after total parathyroidectomy for renal osteodystrophy. Int J Urol, 2000, 7(2): 35-40.
29.	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.
30.	Florakis D, Karakozis S, Tseleni-Balafouta S, et al. Lessons learned from the management of hungry bone syndrome following the removal of an atypical parathyroid adenoma. J Musculoskelet Neuronal Interact, 2019, 19(3): 379-384.
31.	Anwar F, Abraham J, Nakshabandi A, et al. Treatment of hypocalcemia in hungry bone syndrome: A case report. Int J Surg Case Rep, 2018, 51: 335-339.
32.	Levine BS, Coburn JW. Magnesium, the mimic/antagonist to calcium. N Engl J Med, 1984, 310(19): 1253-1255.
33.	Rude RK, Oldham SB, Sharp CF, et al. Parathyroid hormone secretion in magnesium deficiency. J Clin Endocrinol Metab, 1978, 47(4): 800-806.
34.	Rude RK, Oldham SB, Singer FR. Functional hypoparathyroidism and parathyroid hormone end-organ resistance in human magnesium deficiency. Clin Endocrinol (Oxf), 1976, 5(3): 209-224.
35.	夏维波, 章振林, 林华等. 维生素 D 及其类似物的临床应用共识. 中华骨质疏松和骨矿盐疾病杂志, 2018, 11(1): 1-19.
36.	Rolighed L, Rejnmark L, Sikjaer T, et al. Vitamin D treatment in primary hyperparathyroidism: a randomized placebo controlled trial. J Clin Endocrinol Metab, 2014, 99(3): 1072-1080.
37.	Kaderli RM, Riss P, Dunkler D, et al. The impact of vitamin D status on hungry bone syndrome after surgery for primary hyperparathyroidism. Eur J Endocrinol, 2018, 178(1): 1-9.
38.	Boyle IT, Fogelman I, Boyce B, et al. 1-alpha-hydroxyvitamin D3 in primary hyperparathyroidism. Clin Endocrinol (Oxf), 1977, 7 Suppl: 215s-222s.
39.	Heath DA, Van’t Hoff W, Barnes AD, et al. Value of 1-alpha-hydroxy vitamin D3 in treatment of primary hyperparathyroidism before parathyroidectomy. Br Med J, 1979, 1(6161): 450-452.
40.	Agarwal G, Mishra SK, Kar DK, et al. Recovery pattern of patients with osteitis fibrosa cystica in primary hyperparathyroidism after successful parathyroidectomy. Surgery, 2002, 132(6): 1075-1083.

1. Albright F, Reifenstein EC Jr. The Parathyroid glands and metabolic bone disease. Gastroenterology, 1950, 14(4): 594-595.
2. 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.
3. Chen P, Satterwhite JH, Licata AA, et al. Early changes in biochemical markers of bone formation predict BMD response to teriparatide in postmenopausal women with osteoporosis. J Bone Miner Res, 2005, 20(6): 962-970.
4. Silva BC, Bilezikian JP. Parathyroid hormone: anabolic and catabolic actions on the skeleton. Curr Opin Pharmacol, 2015, 22: 41-50.
5. Ma YL, Cain RL, Halladay DL, et al. Catabolic effects of continuous human PTH (1-38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation. Endocrinology, 2001, 142(9): 4047-4054.
6. Liu S, Zhu W, Li S, et al. The effect of bovine parathyroid hormone withdrawal on MC3T3-E1 cell proliferation and phosphorus metabolism. PLoS One, 2015, 10(3): e0120402.
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.
8. Jain N, Reilly RF. Hungry bone syndrome. Curr Opin Nephrol Hypertens, 2017, 26(4): 250-255.
9. Jakubauskas M, Beiša V, Strupas K. Risk factors of developing the hungry bone syndrome after parathyroidectomy for primary hyperparathyroidism. Acta Med Litu, 2018, 25(1): 45-51.
10. Goldfarb M, Gondek SS, Lim SM, et al. Postoperative hungry bone syndrome in patients with secondary hyperparathyroidism of renal origin. World J Surg, 2012, 36(6): 1314-1319.
11. 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.
12. Brasier AR, Nussbaum SR. Hungry bone syndrome: clinical and biochemical predictors of its occurrence after parathyroid surgery. Am J Med, 1988, 84(4): 654-660.
13. Guillén Martínez AJ, Smilg Nicolás C, Moraleda Deleito J, et al. Risk factors and evolution of calcium and parathyroid hormone levels in hungry bone syndrome after parthyroidectomy for primary hyperparathyroidism. Endocrinol Diabetes Nutr, 2020, 67(5): 310-316.
14. Yang G, Zha X, Mao H, et al. Hypocalcemia-based prediction of hungry bone syndrome after parathyroidectomy in hemodialysis patients with refractory secondary hyperparathyroidism. J Int Med Res, 2018, 46(12): 4985-4994.
15. 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.
16. Ho LY, Wong PN, Sin HK, et al. Risk factors and clinical course of hungry bone syndrome after total parathyroidectomy in dialysis patients with secondary hyperparathyroidism. BMC Nephrol, 2017, 18(1): 12.
17. Wang M, Chen B, Zou X, et al. A Nomogram to predict hungry bone syndrome after parathyroidectomy in patients with secondary hyperparathyroidism. J Surg Res, 2020, 255: 33-41.
18. Karunakaran P, Maharajan C, Ramalingam S, et al. Is hungry bone syndrome a cause of postoperative hypocalcemia after total thyroidectomy in thyrotoxicosis? A prospective study with bone mineral density correlation. Surgery, 2018, 163(2): 367-372.
19. See AC, Soo KC. Hypocalcaemia following thyroidectomy for thyrotoxicosis. Br J Surg, 1997, 84(1): 95-97.
20. Garla VV, Salim S, Kovvuru KR, et al. Hungry bone syndrome secondary to prostate cancer successfully treated with radium therapy. BMJ Case Rep, 2018, 2018: bcr2018225039.
21. Sakai K, Tomoda Y, Saito H, et al. Hungry bone syndrome and osteoblastic bone metastasis from gastric cancer. QJM, 2020, hcaa125. [Online ahead of print].
22. Isk Y, Goktas U, Yuzkat N, et al. Hungry bone syndrome as a cause of recurrent laryngospasm after parathyroidectomy. Eur J Anaesthesiol, 2011, 28(2): 142-143.
23. 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.
24. Turner J, Gittoes N, Selby P. Society for Endocrinology Clinical Committee. Society for Endocrinology Endocrine Emergency Guidance: Emergency management of acute hypocalcaemia in adult patients. Endocr Connect, 2016, 5(5): G7-G8.
25. 卢春燕, 李志辉, 朱精强, 等. 术后甲状旁腺机能减退症的诊断及处理. 中国普外基础与临床杂志, 2014, 21(4): 501-506.
26. Ureña P, Basile C, Grateau G, et al. Short-term effects of parathyroidectomy on plasma biochemistry in chronic uremia. Kidney Int, 1989, 36(1): 120-126.
27. 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.
28. Nakagawa M, Emoto A, Nasu N, et al. Calcium supplement necessary to correct hypocalcemia after total parathyroidectomy for renal osteodystrophy. Int J Urol, 2000, 7(2): 35-40.
29. 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.
30. Florakis D, Karakozis S, Tseleni-Balafouta S, et al. Lessons learned from the management of hungry bone syndrome following the removal of an atypical parathyroid adenoma. J Musculoskelet Neuronal Interact, 2019, 19(3): 379-384.
31. Anwar F, Abraham J, Nakshabandi A, et al. Treatment of hypocalcemia in hungry bone syndrome: A case report. Int J Surg Case Rep, 2018, 51: 335-339.
32. Levine BS, Coburn JW. Magnesium, the mimic/antagonist to calcium. N Engl J Med, 1984, 310(19): 1253-1255.
33. Rude RK, Oldham SB, Sharp CF, et al. Parathyroid hormone secretion in magnesium deficiency. J Clin Endocrinol Metab, 1978, 47(4): 800-806.
34. Rude RK, Oldham SB, Singer FR. Functional hypoparathyroidism and parathyroid hormone end-organ resistance in human magnesium deficiency. Clin Endocrinol (Oxf), 1976, 5(3): 209-224.
35. 夏维波, 章振林, 林华等. 维生素 D 及其类似物的临床应用共识. 中华骨质疏松和骨矿盐疾病杂志, 2018, 11(1): 1-19.
36. Rolighed L, Rejnmark L, Sikjaer T, et al. Vitamin D treatment in primary hyperparathyroidism: a randomized placebo controlled trial. J Clin Endocrinol Metab, 2014, 99(3): 1072-1080.
37. Kaderli RM, Riss P, Dunkler D, et al. The impact of vitamin D status on hungry bone syndrome after surgery for primary hyperparathyroidism. Eur J Endocrinol, 2018, 178(1): 1-9.
38. Boyle IT, Fogelman I, Boyce B, et al. 1-alpha-hydroxyvitamin D3 in primary hyperparathyroidism. Clin Endocrinol (Oxf), 1977, 7 Suppl: 215s-222s.
39. Heath DA, Van’t Hoff W, Barnes AD, et al. Value of 1-alpha-hydroxy vitamin D3 in treatment of primary hyperparathyroidism before parathyroidectomy. Br Med J, 1979, 1(6161): 450-452.
40. Agarwal G, Mishra SK, Kar DK, et al. Recovery pattern of patients with osteitis fibrosa cystica in primary hyperparathyroidism after successful parathyroidectomy. Surgery, 2002, 132(6): 1075-1083.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Postoperative hungry bone syndrome

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