Abstract
This study aim s, primarily, to identify the incidence of hungry bone syndrome in parathyroidectomy and, secondarily, to systematically determine the factors predisposing to hungry bone syndrome. PubMed, Embase and Cochrane databases were searched for the data extraction. Human studies reporting risk factors for developing HBS in patients undergoing parathyroidectomy for primary (PHP), secondary (SHP) or tertiary hyperparathyroidism (THP) were included. Newcastle–Ottawa score was used to assess the quality of studies. PROSPERO registration CRD42022293002. This systematic review comprised 2598 patients in the 18 included comparative studies. The overall incidence of HBS following parathyroidectomy in PHP, SHP and THP was 15.9% (8.6–39.1, CI 95%), 43.6% (20.6–87.8, CI 95%) and 12.4% (6.03–32.4, CI 95%), respectively. Younger age group (PHP and SHP), thyroidectomy along with parathyroidectomy (PHP), longer duration of surgery (PHP), larger and heavier resected parathyroids (PHP and SHP), previous dialysis (SHP), longer duration of dialysis (SHP), preoperative cinacalcet (THP) and bisphosphonates use (protective effect) (PHP and THP), calcium levels close to normal (SHP), higher values of parathormone (PHP and SHP), > 90% drop in PTH after surgery (PHP and SHP), raised ALP (PHP and SHP), higher osteocalcin (PHP and SHP), lower albumin (PHP and SHP), higher TRAP 5b (SHP), higher P1NP (PHP), BALP (PHP) and testosterone (PHP) were predictors of HBS. The risk factors for developing hypocalcaemia and HBS should be actively monitored. A complete and accurate recording of the parameters is encouraged among the clinicians to understand the HBS further.
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Data Availability
The data used for this systematic review is available with the corresponding author. The data shall be provided upon reasonable request.
References
Brasier AR, Nussbaum SR (1988) Hungry bone syndrome: clinical and biochemical predictors of its occurrence after parathyroid surgery. Am J Med 84(4):654–660
Ho LY, Wong PN, Sin HK, Wong YY, Lo KC, Chan SF et al (2017) Risk factors and clinical course of hungry bone syndrome after total parathyroidectomy in dialysis patients with secondary hyperparathyroidism. BMC Nephrol 18(1):12
Westerdahl J, Lindblom P, Valdemarsson S, Tibblin S, Bergenfelz A (2000) Risk factors for postoperative hypocalcemia after surgery for primary hyperparathyroidism. Arch Surg 135(2):142–147
Zamboni WA, Folse R (1986) Adenoma weight: a predictor of transient hypocalcemia after parathyroidectomy. Am J Surg 152(6):611–615
Norman JG, Politz DE (2007) Safety of immediate discharge after parathyroidectomy: a prospective study of 3,000 consecutive patients. Endocr Pract Off J Am Coll Endocrinol Am Assoc Clin Endocrinol 13(2):105–113
Wong WK, Wong NA, Farndon JR (1996) Early postoperative plasma calcium concentration as a predictor of the need for calcium supplement after parathyroidectomy. Br J Surg 83(4):532–534
Chia SH, Weisman RA, Tieu D, Kelly C, Dillmann WH, Orloff LA (2006) Prospective study of perioperative factors predicting hypocalcemia after thyroid and parathyroid surgery. Arch Otolaryngol Head Neck Surg 132(1):41–45
Stewart ZA, Blackford A, Somervell H, Friedman K, Garrett-Mayer E, Dackiw APB, et al (2005) 25-hydroxyvitamin D deficiency is a risk factor for symptoms of postoperative hypocalcemia and secondary hyperparathyroidism after minimally invasive parathyroidectomy. Surgery. 138(6):1018–25; discussion 1025–1026
Shea BJ, Reeves BC, Wells G, Thuku M, Hamel C, Moran J et al (2017) AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ 21(358):j4008
Bramer WM, Rethlefsen ML, Kleijnen J, Franco OH (2017) Optimal database combinations for literature searches in systematic reviews: a prospective exploratory study. Syst Rev 6(1):245
MEDICALC :: Medical Calculator System :::: by SCYMED :: Medical Decision Systems :::: [Internet]. [cited 2022 Jun 4]. http://www.scymed.com/en/smnxfd/smnxfdaz.htm
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, The PRISMA et al (2020) statement: an updated guideline for reporting systematic reviews. BMJ 2021:372
GuillénMartínez AJ, SmilgNicolás C, MoraledaDeleito J, GuillénMartínez S, García-Purriños GF (2020) Risk factors and evolution of calcium and parathyroid hormone levels in hungry bone syndrome after parthyroidectomy for primary hyperparathyroidism. Endocrinol Diabetes Nutr 67(5):310–316
Salman MA, Rabiee A, Salman AA, Youssef A, Shaaban HED, Ftohy T, Maurice KK, Balamoun H et al (2022) Role of vitamin D supplements in prevention of hungry bone syndrome after successful parathyroidectomy for primary hyperparathyroidism: a prospective study. Scand J Surg SJS Off Organ Finn Surg Soc Scand Surg Soc [Internet]. 2021 Sep [cited 2022 Jun 3];110(3). https://pubmed.ncbi.nlm.nih.gov/33019891/
Jakubauskas M, Beiša V, Strupas K (2018) Risk factors of developing the hungry bone syndrome after parathyroidectomy for primary hyperparathyroidism. Acta Medica Litu 25(1):45–51
Lee IT, Sheu WHH, Tu ST, Kuo SW, Pei D (2006) Bisphosphonate pretreatment attenuates hungry bone syndrome postoperatively in subjects with primary hyperparathyroidism. J Bone Miner Metab 24(3):255–258
Williams-Karnesky RL, Krumeich L, Wachtel H, Fraker DL, Wirtalla C, Venuto FA et al (2022) Data to inform counseling on parathyroidectomy for secondary hyperparathyroidism of renal origin. Surgery 171(1):63–68
Wang M, Chen B, Zou X, Wei T, Gong R, Zhu J et al (2020) A nomogram to predict hungry bone syndrome after parathyroidectomy in patients with secondary hyperparathyroidism. J Surg Res 255:33–41
Kritmetapak K, Kongpetch S, Chotmongkol W, Raruenrom Y, Sangkhamanon S, Pongchaiyakul C (2020) Incidence of and risk factors for post-parathyroidectomy hungry bone syndrome in patients with secondary hyperparathyroidism. Ren Fail 42(1):1118–1126
Ge Y, Yang G, Wang N, Zha X, Yu X, Mao H et al (2019) Bone metabolism markers and hungry bone syndrome after parathyroidectomy in dialysis patients with secondary hyperparathyroidism. Int Urol Nephrol 51(8):1443–1449
Ferreira D, Vilayur E, Gao M, Sankoorikal C, Bendinelli C (2019) Calcitriol loading before total parathyroidectomy with autotransplant in patients with end-stage kidney disease: does it prevent postoperative hypocalcaemia? Intern Med J 49(7):886–893
Yang G, Zha X, Mao H, Yu X, Wang N, Xing C (2018) Hypocalcemia-based prediction of hungry bone syndrome after parathyroidectomy in hemodialysis patients with refractory secondary hyperparathyroidism. J Int Med Res 46(12):4985–4994
Latus J, Roesel M, Fritz P, Braun N, Ulmer C, Steurer W et al (2013) Incidence of and risk factors for hungry bone syndrome in 84 patients with secondary hyperparathyroidism. Int J Nephrol Renov Dis 8(6):131–137
Goldfarb M, Gondek SS, Lim SM, Farra JC, Nose V, Lew JI (2012) Postoperative hungry bone syndrome in patients with secondary hyperparathyroidism of renal origin. World J Surg 36(6):1314–1319
Ho LY, Wong PN, Sin HK, Wong YY, Lo KC, Chan SF et al (2017) Risk factors and clinical course of hungry bone syndrome after total parathyroidectomy in dialysis patients with secondary hyperparathyroidism. BMC Nephrol 10(18):12
Somnay YR, Weinlander E, Schneider DF, Sippel RS, Chen H (2014) The effect of cinacalcet (Sensipar®) on intraoperative findings in tertiary hyperparathyroidism patients undergoing parathyroidectomy. Surgery 156(6):1308–1314
Mayilvaganan S, VijayaSarathi HA, Shivaprasad C (2017) Preoperative zoledronic acid therapy prevent hungry bone syndrome in patients with primary hyperparathyroidism. Indian J Endocrinol Metab 21(1):76–79
Davenport A, Stearns MP (2022) Administration of pamidronate helps prevent immediate postparathyroidectomy hungry bone syndrome. Nephrol Carlton Vic [Internet]. 2007 Aug [cited 2022 Jun 3];12(4). https://pubmed.ncbi.nlm.nih.gov/17635755/
Kaya C, Tam AA, Dirikoç A, Kılıçyazgan A, Kılıç M, Türkölmez Ş et al (2016) Hypocalcemia development in patients operated for primary hyperparathyroidism: Can it be predicted preoperatively? Arch Endocrinol Metab 60(5):465–471
Kaderli RM, Riss P, Dunkler D, Pietschmann P, Selberherr A, Scheuba C, et al (2018) The impact of vitamin D status on hungry bone syndrome after surgery for primary hyperparathyroidism. Eur J Endocrinol [Internet]. 2018 Jan [cited 2022 Jun 3];178(1). https://pubmed.ncbi.nlm.nih.gov/28877925/
Lo CY, Tam SC (2001) Parathyroid autotransplantation during thyroidectomy: documentation of graft function. Arch Surg 136(12):1381–1385
Chen CH, Wang PW, Liu RT, Tung SC, Jean WY, Lu YC et al (1996) Ectopic parathyroid adenoma with severe hungry bone syndrome: a case report. Chang Yi Xue Za Zhi 19(2):196–202
Yeşilkaya E, Cinaz P, Bideci A, Camurdan O, Demirel F, Demircan S (2009) Hungry bone syndrome after parathyroidectomy caused by an ectopic parathyroid adenoma. J Bone Miner Metab 27(1):101–104
Zheng CM, Chu P, Wu CC, Ma WY, Hung KC, Hsu YH et al (2012) Association between increased serum osteoprotegerin levels and improvement in bone mineral density after parathyroidectomy in hemodialysis patients. Tohoku J Exp Med 226(1):19–27
Ferrè S, Hoenderop JGJ, Bindels RJM (2012) Sensing mechanisms involved in Ca2+ and Mg2+ homeostasis. Kidney Int 82(11):1157–1166
Lian IA, Åsberg A (2018) Should total calcium be adjusted for albumin? A retrospective observational study of laboratory data from central Norway. BMJ Open 8(4):e017703
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Conceived and designed the analysis: RM, KNR, NMN, AG, HS.
Collected the data: KNR.
Data synthesis: KNR, RM, NMN.
Performed the analysis: KNR, RM, NMN.
Manuscript writing: KNR, RM.
Manuscript review and inputs: RM, KNR, NMN, HS, AG.
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The Manuscript was presented in Asia Pacific Thyroid Society 2023 under Best Paper award category.
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Mehta, R., Rao, K.N., Nagarkar, N.M. et al. Hungry Bone Syndrome Following Parathyroidectomy: a Comprehensive Systematic Review of Risk Factors. Indian J Surg (2023). https://doi.org/10.1007/s12262-023-03853-6
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DOI: https://doi.org/10.1007/s12262-023-03853-6