Surgical management of primary hyperparathyroidism with negative preoperative imaging workup
Abstract Introduction and objective: Once the diagnosis of primary hyperparathyroidism (pHPT) is made, the only curative treatment available is parathyroidectomy. This can be achieved by a bilateral neck exploration or through a minimally invasive parathyroidectomy, in which the only neck compartment explored is the one suspected of having the parathyroid gland causing the pHPT. The results of both techniques are equivalent. However, there is a growing tendency to choose MIP when imaging studies correctly localize the affected gland. When imaging studies are negative or discordant, surgical management causes some controversies. Method: We performed a systematic review of original articles, guidelines, and scientific societies documents related to the management of primary hyperparathyroidism with contradictory or negative preoperative localization. We found 211 studies and selected 2 systematic reviews, 20 original articles, and 4 guidelines. Discussion: Guidelines recommend performing a BNE when preoperative localization fails. In the reviewed literature we observed a growing tendency of requesting further imaging studies to perform a MIP, although the majority of surgeons follow the guidelines. MIP + intraoperative PTH monitoring has been reported to have similar success rates as BNE. Some techniques like 18F-Fluorocholine or 11C-choline PET-TC, radio-guided surgery with an intraoperative gamma camera, and intraoperative PTH monitoring, are especially useful in the preoperative workup and as support during surgery when localizing imaging tests result negative Keywords: Hyperparathyroidism, Primary; Parathyroidectomy; Diagnostic imaging
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Noltes ME, Kruijff S, Jansen L, Westerlaan HE, Zandee WT, Dierckx RAJO et al. A retrospective analysis of the diagnostic performance of 11C-choline PET/CT for detection of hyperfunctioning parathyroid glands after prior negative or discordant imaging in primary hyperparathyroidism. EJNMMI Res. 2021;11(32). https://doi.org/10.1186/s13550-021-00778-7
Kim WW, Lee YM, Sung TY, Chung KW, Hong SJ. Selection of parathyroidectomy methods for primary hyperparathyroidism according to concordance between ultrasonography and MIBI scan results. Gland Surg. 2021;10(1):298-306. https://doi.org/10.21037/gs-20-611
Uludag M. Preoperative Localization Studies in Primary Hyperparathyroidism. Med Bull Sisli Etfal Hosp. 2019;53(1):7–15. https://doi.org/10.14744/SEMB.2019.78476
Wilhelm SM, Wang TS, Ruan DT, Lee JA, Asa SL, Duh QY et al. The American Association of Endocrine Surgeons Guidelines for Definitive Management of Primary Hyperparathyroidism. JAMA Surgery. 2016;151(10):959–68. https://doi.org/10.1001/jamasurg.2016.2310
Bilezikian JP, Khan AA, Potts JT Jr. Guidelines for the Management of Asymptomatic Primary Hyperparathyroidism: Summary Statement from the Third International Workshop. The Journal of Clinical Endocrinology & Metabolism. 2009;94(2):335-9. https://doi.org/10.1210/jc.2008-1763
Villar-del-Moral J, Capela-Costa J, Jiménez-García A, Sitges-Serra A, Casanova-Rituerto D, Rocha J et al. Compliance with recommendations on surgery for primary hyperparathyroidism—from guidelines to real practice: results from an Iberian survey. Langenbecks Arch Surg. 2016;401:953–63. https://doi.org/10.1007/s00423-015-1362-3
Aygün N, ??gör A, Uluda? M. The Effectiveness of Preoperative Ultrasonography and Scintigraphy in the Pathological Gland Localization in Primary Hyperparathyroidism Patients. Med Bull Sisli Etfal Hosp. 2019;53(4):379-84. https://doi.org/10.14744/SEMB.2019.37097
Minisola S, Cipriani C, Pepe J. Parathyroid imaging and successful Parathyroidectomy. Clinical Endocrinology. 2015;83:616-7. https://doi.org/10.1111/cen.12880
Alves-Coelho MC, Oliveira NA, Morais S, Beuren AC, Bertolino-Lopes C, Vicente-Santos C et al. Role of imaging tests for preoperative location of pathologic parathyroid tissue in patients with primary hyperparathyroidism. Endocrine Practice. 2016;22(9):1062-7. https://doi.org/10.4158/EP151137.OR
Nehs MA, Ruan DT, Gawande AA, Moore FD Jr, Cho NL. Bilateral neck exploration decreases operative time compared to minimally invasive parathyroidectomy in patients with discordant imaging. World J Surg. 2013;37(7):1614-7. https://doi.org/10.1007/s00268-013-2007-8
Noureldine SI, Gooi Z, Tufano RP. Minimally invasive parathyroid surgery. Gland Surg 2015;4(5):410-9. https://doi.org/10.3978/j.issn.2227-684X.2015.03.07
Barczynski M, Konturek A, Cicho S, Hubalewska-Dydejczyk A, Golkowski F, Huszno B. Intraoperative parathyroid hormone assay improves outcomes of minimally invasive parathyroidectomy mainly in patients with a presumed solitary parathyroid adenoma and missing concordance of preoperative imaging. Clinical Endocrinology. 2007;66:878-85. https://doi.org/10.1111/j.1365-2265.2007.02827.x
Sagan D, Rejdak K, Sak J, Drop A. Nuclear Mapping in Parathyroidectomy: the Impact on Operative Time. Acta Chirurgica Belgica. 2011;111(3):155-60. https://doi.org/10.1080/00015458.2011.11680727
Iacobone M, Scerrino G, Palazzo FF. Parathyroid surgery: an evidence-based volume-outcomes analysis. Langenbecks Arch Surg. 2019;404:919-27. https://doi.org/10.1007/s00423-019-01823-9
Noltes ME, Brands S, Dierckx RAJO, Jager PL, Kelder W, Brouwers AH et al. Non-adherence to consensus guidelines on preoperative imaging in surgery for primary hyperparathyroidism. Laryngoscope Investigative Otolaryngology. 2020;5:1247-53. https://doi.org/10.1002/lio2.464
Grimaldi S, Young J, Kamenicky P, Hartl D, Terroir M, Leboulleux S et al. Challenging pre-surgical localization of hyperfunctioning parathyroid glands in primary hyperparathyroidism: the added value of 18F-Fluorocholine PET/CT. Eur J Nucl Med Mol Imaging. 2018;45:1772–80. https://doi.org/10.1007/s00259-018-4018-z
Scattergood S, Marsden M, Kyrimi E, Ishii H, Doddi S, Sinha P. Combined ultrasound and Sestamibi scintigraphy provides accurate preoperative localisation for patients with primary hyperparathyroidism. Ann R Coll Surg Engl. 2019;101(2):97-102. https://doi.org/10.1308/rcsann.2018.0158
Michaud L, Balogova S, Burgess A, Ohnona J, Huchet V, Kerrou K et al. A Pilot Comparison of 18F-fluorocholine PET/CT, Ultrasonography and 123I/99mTc-sestaMIBI Dual-Phase Dual-Isotope Scintigraphy in the Preoperative Localization of Hyperfunctioning Parathyroid Glands in Primary or Secondary Hyperparathyroidism. Medicine. 2015;94(41):1701 https://doi.org/10.1097/MD.0000000000001701
Khafif A, Masalha M, Landsberg R, Domanchevsky L, Bernstine H, Groshar D et al. The role of F18-fluorocholine positron emission tomography/magnetic resonance imaging in localizing parathyroid adenomas. Eur Arch Otorhinolaryngol. 2019;276:1509–16. https://doi.org/10.1007/s00405-019-05301-2
Ebner Y, Garti-Gross Y, Margulis A, Levy Y, Nabrisky D, Ophir D et al. Parathyroid surgery: correlation between pre-operative localization studies and surgical outcomes. Clinical Endocrinology. 2015;83(5):733-8. https://doi.org/10.1111/cen.12835
Walsh NJ, Sullivan BT, Duke WS, Terris DJ. Routine bilateral neck exploration and four-gland dissection remains unnecessary in modern parathyroid surgery. Laryngoscope Investig Otolaryngology. 2018;4(1):188-92. https://doi.org/10.1002/lio2.223
Scott-Coombes DM, Rees J, Jones G, Stechman MJ. Is Unilateral Neck Surgery Feasible in Patients with Sporadic Primary Hyperparathyroidism and Double Negative Localisation? World J Surg. 2017;41(6):1494-9. https://doi.org/10.1007/s00268-017-3891-0
Quinn AJ, Ryan ÉJ, Garry S, James DL, Boland MR, Young O et al. Use of Intraoperative Parathyroid Hormone in Minimally Invasive Parathyroidectomy for Primary Hyperparathyroidism: A Systematic Review and Meta-analysis. JAMA Otolaryngol Head Neck Surg. 2021;147(2):135-43. https://doi.org/10.1001/jamaoto.2020.4021
Calò PG, Medas F, Loi G, Erdas E, Pisano G, Nicolosi A. Feasibility of unilateral parathyroidectomy in patients with primary hyperparathyroidism and negative or discordant localization studies. Updates Surg. 2016;68(2):155-61. https://doi.org/10.1007/s13304-015-0342-z
Dralle H, Hein J. Parathyreoidektomie bei unklarer Lokalisation. Chirurg. 2013;84:598. https://doi.org/10.1007/s00104-013-2545-5
Ryan S, Courtney D, Moriariu J, Timon C. Surgical management of primary hyperparathyroidism. Eur Arch Otorhinolaryngol. 2017;274(12):4225-32. https://doi.org/10.1007/s00405-017-4776-4
Kim WW, Lee YM, Sung TY, Chung KW, Hong SJ. Selection of parathyroidectomy methods for primary hyperparathyroidism according to concordance between ultrasonography and MIBI scan results. Gland Surg. 2021;10(1):298-306. https://doi.org/10.21037/gs-20-611
Uludag M. Preoperative Localization Studies in Primary Hyperparathyroidism. Med Bull Sisli Etfal Hosp. 2019;53(1):7–15. https://doi.org/10.14744/SEMB.2019.78476
Wilhelm SM, Wang TS, Ruan DT, Lee JA, Asa SL, Duh QY et al. The American Association of Endocrine Surgeons Guidelines for Definitive Management of Primary Hyperparathyroidism. JAMA Surgery. 2016;151(10):959–68. https://doi.org/10.1001/jamasurg.2016.2310
Bilezikian JP, Khan AA, Potts JT Jr. Guidelines for the Management of Asymptomatic Primary Hyperparathyroidism: Summary Statement from the Third International Workshop. The Journal of Clinical Endocrinology & Metabolism. 2009;94(2):335-9. https://doi.org/10.1210/jc.2008-1763
Villar-del-Moral J, Capela-Costa J, Jiménez-García A, Sitges-Serra A, Casanova-Rituerto D, Rocha J et al. Compliance with recommendations on surgery for primary hyperparathyroidism—from guidelines to real practice: results from an Iberian survey. Langenbecks Arch Surg. 2016;401:953–63. https://doi.org/10.1007/s00423-015-1362-3
Aygün N, ??gör A, Uluda? M. The Effectiveness of Preoperative Ultrasonography and Scintigraphy in the Pathological Gland Localization in Primary Hyperparathyroidism Patients. Med Bull Sisli Etfal Hosp. 2019;53(4):379-84. https://doi.org/10.14744/SEMB.2019.37097
Minisola S, Cipriani C, Pepe J. Parathyroid imaging and successful Parathyroidectomy. Clinical Endocrinology. 2015;83:616-7. https://doi.org/10.1111/cen.12880
Alves-Coelho MC, Oliveira NA, Morais S, Beuren AC, Bertolino-Lopes C, Vicente-Santos C et al. Role of imaging tests for preoperative location of pathologic parathyroid tissue in patients with primary hyperparathyroidism. Endocrine Practice. 2016;22(9):1062-7. https://doi.org/10.4158/EP151137.OR
Nehs MA, Ruan DT, Gawande AA, Moore FD Jr, Cho NL. Bilateral neck exploration decreases operative time compared to minimally invasive parathyroidectomy in patients with discordant imaging. World J Surg. 2013;37(7):1614-7. https://doi.org/10.1007/s00268-013-2007-8
Noureldine SI, Gooi Z, Tufano RP. Minimally invasive parathyroid surgery. Gland Surg 2015;4(5):410-9. https://doi.org/10.3978/j.issn.2227-684X.2015.03.07
Barczynski M, Konturek A, Cicho S, Hubalewska-Dydejczyk A, Golkowski F, Huszno B. Intraoperative parathyroid hormone assay improves outcomes of minimally invasive parathyroidectomy mainly in patients with a presumed solitary parathyroid adenoma and missing concordance of preoperative imaging. Clinical Endocrinology. 2007;66:878-85. https://doi.org/10.1111/j.1365-2265.2007.02827.x
Sagan D, Rejdak K, Sak J, Drop A. Nuclear Mapping in Parathyroidectomy: the Impact on Operative Time. Acta Chirurgica Belgica. 2011;111(3):155-60. https://doi.org/10.1080/00015458.2011.11680727
Iacobone M, Scerrino G, Palazzo FF. Parathyroid surgery: an evidence-based volume-outcomes analysis. Langenbecks Arch Surg. 2019;404:919-27. https://doi.org/10.1007/s00423-019-01823-9
Noltes ME, Brands S, Dierckx RAJO, Jager PL, Kelder W, Brouwers AH et al. Non-adherence to consensus guidelines on preoperative imaging in surgery for primary hyperparathyroidism. Laryngoscope Investigative Otolaryngology. 2020;5:1247-53. https://doi.org/10.1002/lio2.464
Grimaldi S, Young J, Kamenicky P, Hartl D, Terroir M, Leboulleux S et al. Challenging pre-surgical localization of hyperfunctioning parathyroid glands in primary hyperparathyroidism: the added value of 18F-Fluorocholine PET/CT. Eur J Nucl Med Mol Imaging. 2018;45:1772–80. https://doi.org/10.1007/s00259-018-4018-z
Scattergood S, Marsden M, Kyrimi E, Ishii H, Doddi S, Sinha P. Combined ultrasound and Sestamibi scintigraphy provides accurate preoperative localisation for patients with primary hyperparathyroidism. Ann R Coll Surg Engl. 2019;101(2):97-102. https://doi.org/10.1308/rcsann.2018.0158
Michaud L, Balogova S, Burgess A, Ohnona J, Huchet V, Kerrou K et al. A Pilot Comparison of 18F-fluorocholine PET/CT, Ultrasonography and 123I/99mTc-sestaMIBI Dual-Phase Dual-Isotope Scintigraphy in the Preoperative Localization of Hyperfunctioning Parathyroid Glands in Primary or Secondary Hyperparathyroidism. Medicine. 2015;94(41):1701 https://doi.org/10.1097/MD.0000000000001701
Khafif A, Masalha M, Landsberg R, Domanchevsky L, Bernstine H, Groshar D et al. The role of F18-fluorocholine positron emission tomography/magnetic resonance imaging in localizing parathyroid adenomas. Eur Arch Otorhinolaryngol. 2019;276:1509–16. https://doi.org/10.1007/s00405-019-05301-2
Ebner Y, Garti-Gross Y, Margulis A, Levy Y, Nabrisky D, Ophir D et al. Parathyroid surgery: correlation between pre-operative localization studies and surgical outcomes. Clinical Endocrinology. 2015;83(5):733-8. https://doi.org/10.1111/cen.12835
Walsh NJ, Sullivan BT, Duke WS, Terris DJ. Routine bilateral neck exploration and four-gland dissection remains unnecessary in modern parathyroid surgery. Laryngoscope Investig Otolaryngology. 2018;4(1):188-92. https://doi.org/10.1002/lio2.223
Scott-Coombes DM, Rees J, Jones G, Stechman MJ. Is Unilateral Neck Surgery Feasible in Patients with Sporadic Primary Hyperparathyroidism and Double Negative Localisation? World J Surg. 2017;41(6):1494-9. https://doi.org/10.1007/s00268-017-3891-0
Quinn AJ, Ryan ÉJ, Garry S, James DL, Boland MR, Young O et al. Use of Intraoperative Parathyroid Hormone in Minimally Invasive Parathyroidectomy for Primary Hyperparathyroidism: A Systematic Review and Meta-analysis. JAMA Otolaryngol Head Neck Surg. 2021;147(2):135-43. https://doi.org/10.1001/jamaoto.2020.4021
Calò PG, Medas F, Loi G, Erdas E, Pisano G, Nicolosi A. Feasibility of unilateral parathyroidectomy in patients with primary hyperparathyroidism and negative or discordant localization studies. Updates Surg. 2016;68(2):155-61. https://doi.org/10.1007/s13304-015-0342-z
Dralle H, Hein J. Parathyreoidektomie bei unklarer Lokalisation. Chirurg. 2013;84:598. https://doi.org/10.1007/s00104-013-2545-5
Ryan S, Courtney D, Moriariu J, Timon C. Surgical management of primary hyperparathyroidism. Eur Arch Otorhinolaryngol. 2017;274(12):4225-32. https://doi.org/10.1007/s00405-017-4776-4
Toribio-Ruano, I., García-Martín, M. ., Sánchez-Mora, B. ., & Torrico-Román , P. de J. . (2022). Surgical management of primary hyperparathyroidism with negative preoperative imaging workup . Revista ORL, 13(2), e27570. https://doi.org/10.14201/orl.27570
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