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Long-Term Success of Surgery for Primary Hyperparathyroidism: Focused Exploration using Intraoperative Parathyroid Hormone Monitoring Versus Four-Gland Exploration

  • Wesley Barnes
  • Peter F. Czako
  • Sapna Nagar
Chapter
Part of the Difficult Decisions in Surgery: An Evidence-Based Approach book series (DDSURGERY)

Abstract

Primary hyperparathyroidism is a common problem that is a result of the excessive secretion of parathyroid hormone (PTH) from the parathyroid glands. This is most commonly caused by a single hypersecreting adenomatous gland. Most all patients with primary hyperparathyroidism meet criteria for surgery. The best operation should provide the highest rate of cure with the lowest rate of complications. The standard surgical approach has traditionally been a four-gland exploration. Though this method has endured many years of excellent cure rates, it has been challenged because a long-lasting cure is possible with the removal of a single adenoma in the majority of cases. Thus, a focused exploration via an image-guided, open unilateral exploration employing intraoperative PTH (ioPTH) monitoring has gained popularity over the last two decades. Specifically, ioPTH monitoring has been shown to be paramount to this approach, enabling a more limited exploration by accurately guiding gland excision and predicting postoperative cure. Several large series of focused parathyroid operations have shown excellent, durable cure rates similar to standard four-gland exploration. Focused exploration guided by ioPTH is a safe, effective technique that is recommended for most patients with sporadic primary hyperparathyroidism.

Keywords

Primary hyperparathyroidism Hypercalcemia Four-gland exploration Bilateral neck exploration Focused parathyroidectomy Minimally invasive parathyroidectomy(MIP) Limited parathyroidectomy Intraoperative parathyroid hormone monitoring (IOPTH) 

References

  1. 1.
    Coker LH, Rorie K, Cantley L, Kirkland K, Stump D, Burbank N, et al. Primary hyperparathyroidism, cognition, and health-related quality of life. Ann Surg. 2005;242(5):642–50.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Fraser WD. Hyperparathyroidism. Lancet. 2009;374(9684):145–58.CrossRefPubMedGoogle Scholar
  3. 3.
    Clark OH, Duh QY. Primary hyperparathyroidism. A surgical perspective. Endocrinol Metab Clin N Am. 1989;18(3):701–14.CrossRefGoogle Scholar
  4. 4.
    Wermers RA, Khosla S, Atkinson EJ, Hodgson SF, O'Fallon WM, Melton LJ 3rd. The rise and fall of primary hyperparathyroidism: a population-based study in Rochester, Minnesota, 1965–1992. Ann Intern Med. 1997;126(6):433–40.CrossRefPubMedGoogle Scholar
  5. 5.
    Heath H 3rd, Hodgson SF, Kennedy MA. Primary hyperparathyroidism. Incidence, morbidity, and potential economic impact in a community. N Engl J Med. 1980;302(4):189–93.CrossRefPubMedGoogle Scholar
  6. 6.
    Yeh MW, Ituarte PH, Zhou HC, Nishimoto S, Liu IL, Harari A, et al. Incidence and prevalence of primary hyperparathyroidism in a racially mixed population. J Clin Endocrinol Metab. 2013;98(3):1122–9.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Beard CM, Heath H 3rd, O'Fallon WM, Anderson JA, Earle JD, Melton LJ 3rd. Therapeutic radiation and hyperparathyroidism. A case-control study in Rochester, Minn. Arch Intern Med. 1989;149(8):1887–90.CrossRefPubMedGoogle Scholar
  8. 8.
    Albright F. A page out of the history of hyperparathyroidism. J Clin Endocrinol Metab. 1948;8(8):637–57.CrossRefPubMedGoogle Scholar
  9. 9.
    Clark OH, Wilkes W, Siperstein AE, Duh QY. Diagnosis and management of asymptomatic hyperparathyroidism: safety, efficacy, and deficiencies in our knowledge. J Bone Miner Res. 1991;6(Suppl 2):S135–42. discussion 51–2.PubMedPubMedCentralGoogle Scholar
  10. 10.
    Turken SA, Cafferty M, Silverberg SJ, De La Cruz L, Cimino C, Lange DJ, et al. Neuromuscular involvement in mild, asymptomatic primary hyperparathyroidism. Am J Med. 1989;87(5):553–7.CrossRefPubMedGoogle Scholar
  11. 11.
    Bilezikian JP, Brandi ML, Rubin M, Silverberg SJ. Primary hyperparathyroidism: new concepts in clinical, densitometric and biochemical features. J Intern Med. 2005;257(1):6–17.CrossRefPubMedGoogle Scholar
  12. 12.
    Silverberg SJ, Shane E, Jacobs TP, Siris ES, Gartenberg F, Seldin D, et al. Nephrolithiasis and bone involvement in primary hyperparathyroidism. Am J Med. 1990;89(3):327–34.CrossRefPubMedGoogle Scholar
  13. 13.
    Silverberg SJ, Bilezikian JP. Asymptomatic primary hyperparathyroidism: a medical perspective. Surg Clin North Am. 2004;84(3):787–801.CrossRefPubMedGoogle Scholar
  14. 14.
    Bilezikian JP, Brandi ML, Eastell R, Silverberg SJ, Udelsman R, Marcocci C, et al. Guidelines for the management of asymptomatic primary hyperparathyroidism: summary statement from the Fourth International Workshop. J Clin Endocrinol Metab. 2014;99(10):3561–9.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Rao DS, Honasoge M, Divine GW, Phillips ER, Lee MW, Ansari MR, et al. Effect of vitamin D nutrition on parathyroid adenoma weight: pathogenetic and clinical implications. J Clin Endocrinol Metab. 2000;85(3):1054–8.PubMedGoogle Scholar
  16. 16.
    Kandil E, Tufaro AP, Carson KA, Lin F, Somervell H, Farrag T, et al. Correlation of plasma 25-hydroxyvitamin D levels with severity of primary hyperparathyroidism and likelihood of parathyroid adenoma localization on sestamibi scan. Arch Otolaryngol Head Neck Surg. 2008;134(10):1071–5.CrossRefPubMedGoogle Scholar
  17. 17.
    Silverberg SJ, Clarke BL, Peacock M, Bandeira F, Boutroy S, Cusano NE, et al. Current issues in the presentation of asymptomatic primary hyperparathyroidism: proceedings of the Fourth International Workshop. J Clin Endocrinol Metab. 2014;99(10):3580–94.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Silverberg SJ, Shane E, de la Cruz L, Dempster DW, Feldman F, Seldin D, et al. Skeletal disease in primary hyperparathyroidism. J Bone Miner Res. 1989;4(3):283–91.CrossRefPubMedGoogle Scholar
  19. 19.
    De Geronimo S, Romagnoli E, Diacinti D, D'Erasmo E, Minisola S. The risk of fractures in postmenopausal women with primary hyperparathyroidism. Eur J Endocrinol. 2006;155(3):415–20.CrossRefPubMedGoogle Scholar
  20. 20.
    Khosla S, Melton LJ 3rd, Wermers RA, Crowson CS, O'Fallon W, Riggs B. Primary hyperparathyroidism and the risk of fracture: a population-based study. J Bone Miner Res. 1999;14(10):1700–7.CrossRefPubMedGoogle Scholar
  21. 21.
    Larsson K, Ljunghall S, Krusemo UB, Naessen T, Lindh E, Persson I. The risk of hip fractures in patients with primary hyperparathyroidism: a population-based cohort study with a follow-up of 19 years. J Intern Med. 1993;234(6):585–93.CrossRefPubMedGoogle Scholar
  22. 22.
    Khosla S, Melton J 3rd. Fracture risk in primary hyperparathyroidism. J Bone Miner Res. 2002;17(Suppl 2):N103–7.PubMedGoogle Scholar
  23. 23.
    Rubin MR, Bilezikian JP, McMahon DJ, Jacobs T, Shane E, Siris E, et al. The natural history of primary hyperparathyroidism with or without parathyroid surgery after 15 years. J Clin Endocrinol Metab. 2008;93(9):3462–70.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Sorensen MD, Duh QY, Grogan RH, Tran TC, Stoller ML. Urinary parameters as predictors of primary hyperparathyroidism in patients with nephrolithiasis. J Urol. 2012;187(2):516–21.CrossRefPubMedGoogle Scholar
  25. 25.
    Tassone F, Gianotti L, Emmolo I, Ghio M, Borretta G. Glomerular filtration rate and parathyroid hormone secretion in primary hyperparathyroidism. J Clin Endocrinol Metab. 2009;94(11):4458–61.CrossRefPubMedGoogle Scholar
  26. 26.
    Yu N, Donnan PT, Flynn RW, Murphy MJ, Smith D, Rudman A, et al. Increased mortality and morbidity in mild primary hyperparathyroid patients. The Parathyroid Epidemiology and Audit Research Study (PEARS). Clin Endocrinol. 2010;73(1):30–4.Google Scholar
  27. 27.
    Yu N, Leese GP, Donnan PT. What predicts adverse outcomes in untreated primary hyperparathyroidism? The Parathyroid Epidemiology and Audit Research Study (PEARS). Clin Endocrinol. 2013;79(1):27–34.CrossRefGoogle Scholar
  28. 28.
    Lind L, Hvarfner A, Palmer M, Grimelius L, Akerstrom G, Ljunghall S. Hypertension in primary hyperparathyroidism in relation to histopathology. Eur J Surg. 1991;157(8):457–9.PubMedGoogle Scholar
  29. 29.
    Lind L, Jacobsson S, Palmer M, Lithell H, Wengle B, Ljunghall S. Cardiovascular risk factors in primary hyperparathyroidism: a 15-year follow-up of operated and unoperated cases. J Intern Med. 1991;230(1):29–35.CrossRefPubMedGoogle Scholar
  30. 30.
    Persson A, Bollerslev J, Rosen T, Mollerup CL, Franco C, Isaksen GA, et al. Effect of surgery on cardiac structure and function in mild primary hyperparathyroidism. Clin Endocrinol. 2011;74(2):174–80.CrossRefGoogle Scholar
  31. 31.
    Iwata S, Walker MD, Di Tullio MR, Hyodo E, Jin Z, Liu R, et al. Aortic valve calcification in mild primary hyperparathyroidism. J Clin Endocrinol Metab. 2012;97(1):132–7.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Walker MD, Rundek T, Homma S, DiTullio M, Iwata S, Lee JA, et al. Effect of parathyroidectomy on subclinical cardiovascular disease in mild primary hyperparathyroidism. Eur J Endocrinol. 2012;167(2):277–85.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Adler JT, Sippel RS, Schaefer S, Chen H. Preserving function and quality of life after thyroid and parathyroid surgery. Lancet Oncol. 2008;9(11):1069–75.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Bilezikian JP, Khan AA, Potts JT Jr, Third International Workshop on the Management of Asymptomatic Primary Hyperthyroidism. Guidelines for the management of asymptomatic primary hyperparathyroidism: summary statement from the third international workshop. J Clin Endocrinol Metab. 2009;94(2):335–9.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Siperstein AE, Shen W, Chan AK, Duh QY, Clark OH. Normocalcemic hyperparathyroidism. Biochemical and symptom profiles before and after surgery. Arch Surg. 1992;127(10):1157–6. discussion 61–3.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Silverberg SJ, Bilezikian JP. “Incipient” primary hyperparathyroidism: a “forme fruste” of an old disease. J Clin Endocrinol Metab. 2003;88(11):5348–52.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Tordjman KM, Greenman Y, Osher E, Shenkerman G, Stern N. Characterization of normocalcemic primary hyperparathyroidism. Am J Med. 2004;117(11):861–3.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Scholz DA, Purnell DC. Asymptomatic primary hyperparathyroidism. 10-year prospective study. Mayo Clin Proc. 1981;56(8):473–8.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Rao DS, Wilson RJ, Kleerekoper M, Parfitt AM. Lack of biochemical progression or continuation of accelerated bone loss in mild asymptomatic primary hyperparathyroidism: evidence for biphasic disease course. J Clin Endocrinol Metab. 1988;67(6):1294–8.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Silverberg SJ, Brown I, Bilezikian JP. Age as a criterion for surgery in primary hyperparathyroidism. Am J Med. 2002;113(8):681–4.CrossRefPubMedGoogle Scholar
  41. 41.
    Ambrogini E, Cetani F, Cianferotti L, Vignali E, Banti C, Viccica G, et al. Surgery or surveillance for mild asymptomatic primary hyperparathyroidism: a prospective, randomized clinical trial. J Clin Endocrinol Metab. 2007;92(8):3114–21.CrossRefPubMedGoogle Scholar
  42. 42.
    Bollerslev J, Jansson S, Mollerup CL, Nordenstrom J, Lundgren E, Torring O, et al. Medical observation, compared with parathyroidectomy, for asymptomatic primary hyperparathyroidism: a prospective, randomized trial. J Clin Endocrinol Metab. 2007;92(5):1687–92.CrossRefPubMedGoogle Scholar
  43. 43.
    Rao DS, Phillips ER, Divine GW, Talpos GB. Randomized controlled clinical trial of surgery versus no surgery in patients with mild asymptomatic primary hyperparathyroidism. J Clin Endocrinol Metab. 2004;89(11):5415–22.CrossRefPubMedGoogle Scholar
  44. 44.
    Silverberg SJ, Lewiecki EM, Mosekilde L, Peacock M, Rubin MR. Presentation of asymptomatic primary hyperparathyroidism: proceedings of the third international workshop. J Clin Endocrinol Metab. 2009;94(2):351–65.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Udelsman R, Akerstrom G, Biagini C, Duh QY, Miccoli P, Niederle B, et al. The surgical management of asymptomatic primary hyperparathyroidism: proceedings of the Fourth International Workshop. J Clin Endocrinol Metab. 2014;99(10):3595–606.CrossRefPubMedGoogle Scholar
  46. 46.
    Hedback G, Tisell LE, Bengtsson BA, Hedman I, Oden A. Premature death in patients operated on for primary hyperparathyroidism. World J Surg. 1990;14(6):829–35. discussion 36.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Ogard CG, Engholm G, Almdal TP, Vestergaard H. Increased mortality in patients hospitalized with primary hyperparathyroidism during the period 1977–1993 in Denmark. World J Surg. 2004;28(1):108–11.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Sivula A, Pelkonen R. Long-term health risk of primary hyperparathyroidism: the effect of surgery. Ann Med. 1996;28(2):95–100.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Ronni-Sivula H. Causes of death in patients previously operated on for primary hyperparathyroidism. Ann Chir Gynaecol. 1985;74(1):13–8.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Bostrom H, Alveryd A. Stroke in hyperparathyroidism. Acta Med Scand. 1972;192(4):299–308.PubMedGoogle Scholar
  51. 51.
    Palmer M, Adami HO, Bergstrom R, Akerstrom G, Ljunghall S. Mortality after surgery for primary hyperparathyroidism: a follow-up of 441 patients operated on from 1956 to 1979. Surgery. 1987;102(1):1–7.PubMedGoogle Scholar
  52. 52.
    Yeh MW, Wiseman JE, Ituarte PH, Pasternak JD, Hwang RS, Wu B, et al. Surgery for primary hyperparathyroidism: are the consensus guidelines being followed? Ann Surg. 2012;255(6):1179–83.CrossRefPubMedGoogle Scholar
  53. 53.
    Mandel F. Therapeutisher Versuch bein Einem Falls von Ostitis Fibrosa Generalisata Mittles: Extirpation eins Epithelkorperchen Tumors. Wein Klin Wochenshr Zentral. 1926;143:245–84.Google Scholar
  54. 54.
    Kebebew E, Arici C, Duh QY, Clark OH. Localization and reoperation results for persistent and recurrent parathyroid carcinoma. Arch Surg. 2001;136(8):878–85.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Jaskowiak N, Norton JA, Alexander HR, Doppman JL, Shawker T, Skarulis M, et al. A prospective trial evaluating a standard approach to reoperation for missed parathyroid adenoma. Ann Surg. 1996;224(3):308–20. discussion 20–1.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Shen W, Duren M, Morita E, Higgins C, Duh QY, Siperstein AE, et al. Reoperation for persistent or recurrent primary hyperparathyroidism. Arch Surg. 1996;131(8):861–7. discussion 7–9.CrossRefPubMedGoogle Scholar
  57. 57.
    Bruining HA, Birkenhager JC, Ong GL, Lamberts SW. Causes of failure in operations for hyperparathyroidism. Surgery. 1987;101(5):562–5.PubMedGoogle Scholar
  58. 58.
    Schneider DF, Mazeh H, Chen H, Sippel RS. Predictors of recurrence in primary hyperparathyroidism: an analysis of 1386 cases. Ann Surg. 2014;259(3):563–8.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Norman J, Lopez J, Politz D. Abandoning unilateral parathyroidectomy: why we reversed our position after 15,000 parathyroid operations. J Am Coll Surg. 2012;214(3):260–9.CrossRefPubMedGoogle Scholar
  60. 60.
    Udelsman R, Lin Z, Donovan P. The superiority of minimally invasive parathyroidectomy based on 1650 consecutive patients with primary hyperparathyroidism. Ann Surg. 2011;253(3):585–91.CrossRefPubMedGoogle Scholar
  61. 61.
    McGill J, Sturgeon C, Kaplan SP, Chiu B, Kaplan EL, Angelos P. How does the operative strategy for primary hyperparathyroidism impact the findings and cure rate? A comparison of 800 parathyroidectomies. J Am Coll Surg. 2008;207(2):246–9.CrossRefPubMedGoogle Scholar
  62. 62.
    Westerdahl J, Bergenfelz A. Unilateral versus bilateral neck exploration for primary hyperparathyroidism: five-year follow-up of a randomized controlled trial. Ann Surg. 2007;246(6):976–80. discussion 80–1.CrossRefPubMedGoogle Scholar
  63. 63.
    Allendorf J, DiGorgi M, Spanknebel K, Inabnet W, Chabot J, Logerfo P. 1112 consecutive bilateral neck explorations for primary hyperparathyroidism. World J Surg. 2007;31(11):2075–80.CrossRefPubMedGoogle Scholar
  64. 64.
    Bergenfelz A, Lindblom P, Tibblin S, Westerdahl J. Unilateral versus bilateral neck exploration for primary hyperparathyroidism: a prospective randomized controlled trial. Ann Surg. 2002;236(5):543–51.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    van Heerden JA, Grant CS. Surgical treatment of primary hyperparathyroidism: an institutional perspective. World J Surg. 1991;15(6):688–92.CrossRefPubMedGoogle Scholar
  66. 66.
    Clark OH, Way LW, Hunt TK. Recurrent hyperparathyroidism. Ann Surg. 1976;184(4):391–402.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Cooke TJ, Boey JH, Sweeney EC, Gilbert JM, Taylor S. Parathyroidectomy: extent of resection and late results. Br J Surg. 1977;64(3):153–7.CrossRefPubMedGoogle Scholar
  68. 68.
    Rudberg C, Akerstrom G, Palmer M, Ljunghall S, Adami HO, Johansson H, et al. Late results of operation for primary hyperparathyroidism in 441 patients. Surgery. 1986;99(6):643–51.PubMedGoogle Scholar
  69. 69.
    Tibblin S, Bizard JP, Bondeson AG, Bonjer J, Bruining HA, Meier F, et al. Primary hyperparathyroidism due to solitary adenoma. A comparative multicentre study of early and long-term results of different surgical regimens. Eur J Surg. 1991;157(9):511–5.PubMedGoogle Scholar
  70. 70.
    Grant CS, Thompson G, Farley D, van Heerden J. Primary hyperparathyroidism surgical management since the introduction of minimally invasive parathyroidectomy: Mayo Clinic experience. Arch Surg. 2005;140(5):472–8. discussion 8–9.CrossRefPubMedGoogle Scholar
  71. 71.
    Malmaeus J, Granberg PO, Halvorsen J, Akerstrom G, Johansson H. Parathyroid surgery in Scandinavia. Acta Chir Scand. 1988;154(7–8):409–13.PubMedGoogle Scholar
  72. 72.
    Snyder SK, Lairmore TC, Hendricks JC, Roberts JW. Elucidating mechanisms of recurrent laryngeal nerve injury during thyroidectomy and parathyroidectomy. J Am Coll Surg. 2008;206(1):123–30.CrossRefPubMedGoogle Scholar
  73. 73.
    Chen H. Radioguided parathyroid surgery. Adv Surg. 2004;38:377–92.PubMedGoogle Scholar
  74. 74.
    Wang CA. Surgical management of primary hyperparathyroidism. Curr Probl Surg. 1985;22(11):1–50.CrossRefPubMedGoogle Scholar
  75. 75.
    Tibblin S, Bondeson AG, Ljungberg O. Unilateral parathyroidectomy in hyperparathyroidism due to single adenoma. Ann Surg. 1982;195(3):245–52.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Doppman JL. Reoperative parathyroid surgery; localization procedures. Prog Surg. 1986;18:117–32.CrossRefGoogle Scholar
  77. 77.
    Clark OH. Surgical treatment of primary hyperparathyroidism. Adv Endocrinol Metab. 1995;6:1–16.PubMedGoogle Scholar
  78. 78.
    Kunstman JW, Kirsch JD, Mahajan A, Udelsman R. Clinical review: parathyroid localization and implications for clinical management. J Clin Endocrinol Metab. 2013;98(3):902–12.CrossRefPubMedGoogle Scholar
  79. 79.
    Sample WF, Mitchell SP, Bledsoe RC. Parathyroid ultrasonography. Radiology. 1978;127(2):485–90.CrossRefPubMedGoogle Scholar
  80. 80.
    Arima M, Yokoi H, Sonoda T. Preoperative identification of tumor of the parathyroid by ultrasonotomography. Surg Gynecol Obstet. 1975;141(2):242–4.PubMedGoogle Scholar
  81. 81.
    Lucas RJ, Welsh RJ, Glover JL. Unilateral neck exploration for primary hyperparathyroidism. Arch Surg. 1990;125(8):982–4. discussion 4–5.CrossRefPubMedGoogle Scholar
  82. 82.
    Rickes S, Sitzy J, Neye H, Ocran KW, Wermke W. High-resolution ultrasound in combination with colour-Doppler sonography for preoperative localization of parathyroid adenomas in patients with primary hyperparathyroidism. Ultraschall Med. 2003;24(2):85–9.CrossRefPubMedGoogle Scholar
  83. 83.
    Cheung K, Wang TS, Farrokhyar F, Roman SA, Sosa JA. A meta-analysis of preoperative localization techniques for patients with primary hyperparathyroidism. Ann Surg Oncol. 2012;19(2):577–83.CrossRefPubMedGoogle Scholar
  84. 84.
    Ruda JM, Hollenbeak CS, Stack BC Jr. A systematic review of the diagnosis and treatment of primary hyperparathyroidism from 1995 to 2003. Otolaryngol Head Neck Surg. 2005;132(3):359–72.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Berber E, Parikh RT, Ballem N, Garner CN, Milas M, Siperstein AE. Factors contributing to negative parathyroid localization: an analysis of 1000 patients. Surgery. 2008;144(1):74–9.CrossRefPubMedGoogle Scholar
  86. 86.
    Bentrem DJ, Angelos P, Talamonti MS, Nayar R. Is preoperative investigation of the thyroid justified in patients undergoing parathyroidectomy for hyperparathyroidism? Thyroid. 2002;12(12):1109–12.CrossRefPubMedGoogle Scholar
  87. 87.
    Prager G, Czerny C, Ofluoglu S, Kurtaran A, Passler C, Kaczirek K, et al. Impact of localization studies on feasibility of minimally invasive parathyroidectomy in an endemic goiter region. J Am Coll Surg. 2003;196(4):541–8.CrossRefPubMedGoogle Scholar
  88. 88.
    Milas M, Mensah A, Alghoul M, Berber E, Stephen A, Siperstein A, et al. The impact of office neck ultrasonography on reducing unnecessary thyroid surgery in patients undergoing parathyroidectomy. Thyroid. 2005;15(9):1055–9.CrossRefPubMedGoogle Scholar
  89. 89.
    Morita SY, Somervell H, Umbricht CB, Dackiw AP, Zeiger MA. Evaluation for concomitant thyroid nodules and primary hyperparathyroidism in patients undergoing parathyroidectomy or thyroidectomy. Surgery. 2008;144(6):862–6. discussion 6–8.CrossRefPubMedGoogle Scholar
  90. 90.
    De Feo ML, Colagrande S, Biagini C, Tonarelli A, Bisi G, Vaggelli L, et al. Parathyroid glands: combination of (99m)Tc MIBI scintigraphy and US for demonstration of parathyroid glands and nodules. Radiology. 2000;214(2):393–402.CrossRefPubMedGoogle Scholar
  91. 91.
    Haber RS, Kim CK, Inabnet WB. Ultrasonography for preoperative localization of enlarged parathyroid glands in primary hyperparathyroidism: comparison with (99m)technetium sestamibi scintigraphy. Clin Endocrinol. 2002;57(2):241–9.CrossRefGoogle Scholar
  92. 92.
    Reeder SB, Desser TS, Weigel RJ, Jeffrey RB. Sonography in primary hyperparathyroidism: review with emphasis on scanning technique. J Ultrasound Med. 2002;21(5):539–52. quiz 53–4.CrossRefPubMedGoogle Scholar
  93. 93.
    Gilat H, Cohen M, Feinmesser R, Benzion J, Shvero J, Segal K, et al. Minimally invasive procedure for resection of a parathyroid adenoma: the role of preoperative high-resolution ultrasonography. J Clin Ultrasound. 2005;33(6):283–7.CrossRefPubMedGoogle Scholar
  94. 94.
    Young AE, Gaunt JI, Croft DN, Collins RE, Wells CP, Coakley AJ. Location of parathyroid adenomas by thallium-201 and technetium-99m subtraction scanning. Br Med J. 1983;286(6375):1384–6.CrossRefGoogle Scholar
  95. 95.
    Coakley AJ, Kettle AG, Wells CP, O'Doherty MJ, Collins RE. 99Tcm sestamibi—a new agent for parathyroid imaging. Nucl Med Commun. 1989;10(11):791–4.CrossRefPubMedGoogle Scholar
  96. 96.
    Gotthardt M, Lohmann B, Behr TM, Bauhofer A, Franzius C, Schipper ML, et al. Clinical value of parathyroid scintigraphy with technetium-99m methoxyisobutylisonitrile: discrepancies in clinical data and a systematic metaanalysis of the literature. World J Surg. 2004;28(1):100–7.CrossRefPubMedGoogle Scholar
  97. 97.
    Mihai R, Gleeson F, Buley ID, Roskell DE, Sadler GP. Negative imaging studies for primary hyperparathyroidism are unavoidable: correlation of sestamibi and high-resolution ultrasound scanning with histological analysis in 150 patients. World J Surg. 2006;30(5):697–704.CrossRefPubMedGoogle Scholar
  98. 98.
    Erbil Y, Barbaros U, Yanik BT, Salmaslioglu A, Tunaci M, Adalet I, et al. Impact of gland morphology and concomitant thyroid nodules on preoperative localization of parathyroid adenomas. Laryngoscope. 2006;116(4):580–5.CrossRefPubMedGoogle Scholar
  99. 99.
    Vattimo A, Bertelli P, Cintorino M, Burroni L, Volterrani D, Vella A, et al. Hurthle cell tumor dwelling in hot thyroid nodules: preoperative detection with technetium-99m-MIBI dual-phase scintigraphy. Journal of nuclear medicine : official publication. Soc Nucl Med. 1998;39(5):822–5.Google Scholar
  100. 100.
    Siperstein A, Berber E, Mackey R, Alghoul M, Wagner K, Milas M. Prospective evaluation of sestamibi scan, ultrasonography, and rapid PTH to predict the success of limited exploration for sporadic primary hyperparathyroidism. Surgery. 2004;136(4):872–80.CrossRefPubMedGoogle Scholar
  101. 101.
    Wong KK, Fig LM, Gross MD, Dwamena BA. Parathyroid adenoma localization with 99mTc-sestamibi SPECT/CT: a meta-analysis. Nucl Med Commun. 2015;36(4):363–75.CrossRefPubMedGoogle Scholar
  102. 102.
    Lavely WC, Goetze S, Friedman KP, Leal JP, Zhang Z, Garret-Mayer E, et al. Comparison of SPECT/CT, SPECT, and planar imaging with single- and dual-phase (99m)Tc-sestamibi parathyroid scintigraphy. Journal of nuclear medicine : official publication. Soc Nucl Med. 2007;48(7):1084–9.CrossRefGoogle Scholar
  103. 103.
    Mortenson MM, Evans DB, Lee JE, Hunter GJ, Shellingerhout D, Vu T, et al. Parathyroid exploration in the reoperative neck: improved preoperative localization with 4D-computed tomography. J Am Coll Surg. 2008;206(5):888–95. discussion 95–6.CrossRefPubMedGoogle Scholar
  104. 104.
    Starker LF, Mahajan A, Bjorklund P, Sze G, Udelsman R, Carling T. 4D parathyroid CT as the initial localization study for patients with de novo primary hyperparathyroidism. Ann Surg Oncol. 2011;18(6):1723–8.CrossRefPubMedGoogle Scholar
  105. 105.
    Mahajan A, Starker LF, Ghita M, Udelsman R, Brink JA, Carling T. Parathyroid four-dimensional computed tomography: evaluation of radiation dose exposure during preoperative localization of parathyroid tumors in primary hyperparathyroidism. World J Surg. 2012;36(6):1335–9.CrossRefPubMedGoogle Scholar
  106. 106.
    Patel CN, Salahudeen HM, Lansdown M, Scarsbrook AF. Clinical utility of ultrasound and 99mTc sestamibi SPECT/CT for preoperative localization of parathyroid adenoma in patients with primary hyperparathyroidism. Clin Radiol. 2010;65(4):278–87.CrossRefPubMedGoogle Scholar
  107. 107.
    Chiu B, Sturgeon C, Angelos P. What is the link between nonlocalizing sestamibi scans, multigland disease, and persistent hypercalcemia? A study of 401 consecutive patients undergoing parathyroidectomy. Surgery. 2006;140(3):418–22.CrossRefPubMedGoogle Scholar
  108. 108.
    Arici C, Cheah WK, Ituarte PH, Morita E, Lynch TC, Siperstein AE, et al. Can localization studies be used to direct focused parathyroid operations? Surgery. 2001;129(6):720–9.CrossRefPubMedGoogle Scholar
  109. 109.
    Sugg SL, Krzywda EA, Demeure MJ, Wilson SD. Detection of multiple gland primary hyperparathyroidism in the era of minimally invasive parathyroidectomy. Surgery. 2004;136(6):1303–9.CrossRefPubMedGoogle Scholar
  110. 110.
    Carneiro DM, Solorzano CC, Nader MC, Ramirez M, Irvin GL 3rd. Comparison of intraoperative iPTH assay (QPTH) criteria in guiding parathyroidectomy: which criterion is the most accurate? Surgery. 2003;134(6):973–9. discussion 9–81.CrossRefPubMedGoogle Scholar
  111. 111.
    Haciyanli M, Lal G, Morita E, Duh QY, Kebebew E, Clark OH. Accuracy of preoperative localization studies and intraoperative parathyroid hormone assay in patients with primary hyperparathyroidism and double adenoma. J Am Coll Surg. 2003;197(5):739–46.CrossRefPubMedGoogle Scholar
  112. 112.
    Clerici T, Brandle M, Lange J, Doherty GM, Gauger PG. Impact of intraoperative parathyroid hormone monitoring on the prediction of multiglandular parathyroid disease. World J Surg. 2004;28(2):187–92.CrossRefPubMedGoogle Scholar
  113. 113.
    Riss P, Kaczirek K, Heinz G, Bieglmayer C, Niederle B. A “defined baseline” in PTH monitoring increases surgical success in patients with multiple gland disease. Surgery. 2007;142(3):398–404.CrossRefPubMedGoogle Scholar
  114. 114.
    Siperstein A, Berber E, Barbosa GF, Tsinberg M, Greene AB, Mitchell J, et al. Predicting the success of limited exploration for primary hyperparathyroidism using ultrasound, sestamibi, and intraoperative parathyroid hormone: analysis of 1158 cases. Ann Surg. 2008;248(3):420–8.PubMedGoogle Scholar
  115. 115.
    Barczynski M, Konturek A, Hubalewska-Dydejczyk A, Cichon S, Nowak W. Evaluation of Halle, Miami, Rome, and Vienna intraoperative iPTH assay criteria in guiding minimally invasive parathyroidectomy. Langenbeck’s Arch Surg. 2009;394(5):843–9.CrossRefGoogle Scholar
  116. 116.
    Kaplan EL, Yashiro T, Salti G. Primary hyperparathyroidism in the 1990s. Choice of surgical procedures for this disease. Ann Surg. 1992;215(4):300–17.CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Molinari AS, Irvin GL 3rd, Deriso GT, Bott L. Incidence of multiglandular disease in primary hyperparathyroidism determined by parathyroid hormone secretion. Surgery. 1996;120(6):934–6. discussion 6–7.CrossRefPubMedGoogle Scholar
  118. 118.
    Westerdahl J, Lindblom P, Bergenfelz A. Measurement of intraoperative parathyroid hormone predicts long-term operative success. Arch Surg. 2002;137(2):186–90.CrossRefPubMedGoogle Scholar
  119. 119.
    Vignali E, Picone A, Materazzi G, Steffe S, Berti P, Cianferotti L, et al. A quick intraoperative parathyroid hormone assay in the surgical management of patients with primary hyperparathyroidism: a study of 206 consecutive cases. Eur J Endocrinol. 2002;146(6):783–8.CrossRefPubMedGoogle Scholar
  120. 120.
    Westerdahl J, Bergenfelz A. Sestamibi scan-directed parathyroid surgery: potentially high failure rate without measurement of intraoperative parathyroid hormone. World J Surg. 2004;28(11):1132–8.CrossRefPubMedGoogle Scholar
  121. 121.
    Carneiro-Pla DM, Solorzano CC, Irvin GL 3rd. Consequences of targeted parathyroidectomy guided by localization studies without intraoperative parathyroid hormone monitoring. J Am Coll Surg. 2006;202(5):715–22.CrossRefPubMedGoogle Scholar
  122. 122.
    Norman J. Recent trends becoming standard of care yielding smaller, more successful operations at a lower cost. Otolaryngol Clin N Am. 2004;37(4):683–8. vii.CrossRefGoogle Scholar
  123. 123.
    Chen H, Mack E, Starling JR. Radioguided parathyroidectomy is equally effective for both adenomatous and hyperplastic glands. Ann Surg. 2003;238(3):332–7. discussion 7–8.PubMedPubMedCentralGoogle Scholar
  124. 124.
    Nussbaum SR, Thompson AR, Hutcheson KA, Gaz RD, Wang CA. Intraoperative measurement of parathyroid hormone in the surgical management of hyperparathyroidism. Surgery. 1988;104(6):1121–7.PubMedGoogle Scholar
  125. 125.
    Irvin GL 3rd, Dembrow VD, Prudhomme DL. Operative monitoring of parathyroid gland hyperfunction. Am J Surg. 1991;162(4):299–302.CrossRefPubMedGoogle Scholar
  126. 126.
    James BC, Nagar S, Tracy M, Kaplan EL, Angelos P, Scherberg NH, et al. A novel, ultrarapid parathyroid hormone assay to distinguish parathyroid from nonparathyroid tissue. Surgery. 2014;156(6):1638–43.CrossRefPubMedGoogle Scholar
  127. 127.
    Irvin GL 3rd, Dembrow VD, Prudhomme DL. Clinical usefulness of an intraoperative “quick parathyroid hormone” assay. Surgery. 1993;114(6):1019–22. discussion 22–3.PubMedGoogle Scholar
  128. 128.
    Mazeh H, Chen H, Leverson G, Sippel RS. Creation of a “Wisconsin index” nomogram to predict the likelihood of additional hyperfunctioning parathyroid glands during parathyroidectomy. Ann Surg. 2013;257(1):138–41.CrossRefPubMedGoogle Scholar
  129. 129.
    Kebebew E, Hwang J, Reiff E, Duh QY, Clark OH. Predictors of single-gland vs multigland parathyroid disease in primary hyperparathyroidism: a simple and accurate scoring model. Arch Surg. 2006;141(8):777–82. discussion 82.CrossRefPubMedGoogle Scholar
  130. 130.
    Riss P, Kaczirek K, Bieglmayer C, Niederle B. PTH spikes during parathyroid exploration--a possible pitfall during PTH monitoring? Langenbeck’s Arch Surg. 2007;392(4):427–30.CrossRefGoogle Scholar
  131. 131.
    Chiu B, Sturgeon C, Angelos P. Which intraoperative parathyroid hormone assay criterion best predicts operative success? A study of 352 consecutive patients. Arch Surg. 2006;141(5):483–7. discussion 7–8.CrossRefPubMedGoogle Scholar
  132. 132.
    Cook MR, Pitt SC, Schaefer S, Sippel R, Chen H. A rising ioPTH level immediately after parathyroid resection: are additional hyperfunctioning glands always present? An application of the Wisconsin criteria. Ann Surg. 2010;251(6):1127–30.CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Irvin GL 3rd, Solorzano CC, Carneiro DM. Quick intraoperative parathyroid hormone assay: surgical adjunct to allow limited parathyroidectomy, improve success rate, and predict outcome. World J Surg. 2004;28(12):1287–92.CrossRefPubMedGoogle Scholar
  134. 134.
    Lombardi CP, Raffaelli M, Traini E, Di Stasio E, Carrozza C, De Crea C, et al. Intraoperative PTH monitoring during parathyroidectomy: the need for stricter criteria to detect multiglandular disease. Langenbeck’s Arch Surg. 2008;393(5):639–45.CrossRefGoogle Scholar
  135. 135.
    Weber KJ, Misra S, Lee JK, Wilhelm SW, DeCresce R, Prinz RA. Intraoperative PTH monitoring in parathyroid hyperplasia requires stricter criteria for success. Surgery. 2004;136(6):1154–9.CrossRefPubMedGoogle Scholar
  136. 136.
    Jaskowiak NT, Sugg SL, Helke J, Koka MR, Kaplan EL. Pitfalls of intraoperative quick parathyroid hormone monitoring and gamma probe localization in surgery for primary hyperparathyroidism. Arch Surg. 2002;137(6):659–68. discussion 68–9.CrossRefPubMedGoogle Scholar
  137. 137.
    Gauger PG, Agarwal G, England BG, Delbridge LW, Matz KA, Wilkinson M, et al. Intraoperative parathyroid hormone monitoring fails to detect double parathyroid adenomas: a 2-institution experience. Surgery. 2001;130(6):1005–10.CrossRefPubMedGoogle Scholar
  138. 138.
    Lew JI, Irvin GL 3rd. Focused parathyroidectomy guided by intra-operative parathormone monitoring does not miss multiglandular disease in patients with sporadic primary hyperparathyroidism: a 10-year outcome. Surgery. 2009;146(6):1021–7.CrossRefPubMedGoogle Scholar
  139. 139.
    Lew JI, Rivera M, Irvin GL 3rd, Solorzano CC. Operative failure in the era of focused parathyroidectomy: a contemporary series of 845 patients. Arch Surg. 2010;145(7):628–33.CrossRefPubMedGoogle Scholar
  140. 140.
    Richards ML, Thompson GB, Farley DR, Grant CS. An optimal algorithm for intraoperative parathyroid hormone monitoring. Arch Surg. 2011;146(3):280–5.CrossRefPubMedGoogle Scholar
  141. 141.
    Richards ML, Grant CS. Current applications of the intraoperative parathyroid hormone assay in parathyroid surgery. Am Surg. 2007;73(4):311–7.PubMedGoogle Scholar
  142. 142.
    Hughes DT, Miller BS, Doherty GM, Gauger PG. Intraoperative parathyroid hormone monitoring in patients with recognized multiglandular primary hyperparathyroidism. World J Surg. 2011;35(2):336–41.CrossRefPubMedGoogle Scholar
  143. 143.
    Carneiro-Pla DM, Solorzano CC, Lew JI, Irvin GL 3rd. Long-term outcome of patients with intraoperative parathyroid level remaining above the normal range during parathyroidectomy. Surgery. 2008;144(6):989–93. discussion 93–4.CrossRefPubMedGoogle Scholar
  144. 144.
    Carneiro DM, Solorzano CC, Irvin GL 3rd. Recurrent disease after limited parathyroidectomy for sporadic primary hyperparathyroidism. J Am Coll Surg. 2004;199(6):849–53. discussion 53–5.CrossRefPubMedGoogle Scholar
  145. 145.
    Carneiro DM, Irvin GL 3rd. Late parathyroid function after successful parathyroidectomy guided by intraoperative hormone assay (QPTH) compared with the standard bilateral neck exploration. Surgery. 2000;128(6):925–9. discussion 35–6.CrossRefPubMedGoogle Scholar
  146. 146.
    Barczynski M, Golkowski F, Nawrot I. The current status of intraoperative iPTH assay in surgery for primary hyperparathyroidism. Gland Surg. 2015;4(1):36–43.PubMedPubMedCentralGoogle Scholar
  147. 147.
    Stalberg P, Sidhu S, Sywak M, Robinson B, Wilkinson M, Delbridge L. Intraoperative parathyroid hormone measurement during minimally invasive parathyroidectomy: does it “value-add” to decision-making? J Am Coll Surg. 2006;203(1):1–6.CrossRefPubMedGoogle Scholar
  148. 148.
    Chen H, Pruhs Z, Starling JR, Mack E. Intraoperative parathyroid hormone testing improves cure rates in patients undergoing minimally invasive parathyroidectomy. Surgery. 2005;138(4):583–7. discussion 7–90.CrossRefPubMedGoogle Scholar
  149. 149.
    Venkat R, Kouniavsky G, Tufano RP, Schneider EB, Dackiw AP, Zeiger MA. Long-term outcome in patients with primary hyperparathyroidism who underwent minimally invasive parathyroidectomy. World J Surg. 2012;36(1):55–60.CrossRefPubMedGoogle Scholar
  150. 150.
    Proye CA, Carnaille B, Bizard JP, Quievreux JL, Lecomte-Houcke M. Multiglandular disease in seemingly sporadic primary hyperparathyroidism revisited: where are we in the early 1990s? A plea against unilateral parathyroid exploration. Surgery. 1992;112(6):1118–22.PubMedGoogle Scholar
  151. 151.
    Slepavicius A, Beisa V, Janusonis V, Strupas K. Focused versus conventional parathyroidectomy for primary hyperparathyroidism: a prospective, randomized, blinded trial. Langenbeck’s Arch Surg. 2008;393(5):659–66.CrossRefGoogle Scholar
  152. 152.
    Schneider DF, Mazeh H, Sippel RS, Chen H. Is minimally invasive parathyroidectomy associated with greater recurrence compared to bilateral exploration? Analysis of more than 1,000 cases. Surgery. 2012;152(6):1008–15.CrossRefPubMedPubMedCentralGoogle Scholar
  153. 153.
    Miccoli P, Bendinelli C, Berti P, Vignali E, Pinchera A, Marcocci C. Video-assisted versus conventional parathyroidectomy in primary hyperparathyroidism: a prospective randomized study. Surgery. 1999;126(6):1117–21. discussion 21–2.CrossRefPubMedPubMedCentralGoogle Scholar
  154. 154.
    Irvin GL 3rd, Sfakianakis G, Yeung L, Deriso GT, Fishman LM, Molinari AS, et al. Ambulatory parathyroidectomy for primary hyperparathyroidism. Arch Surg. 1996;131(10):1074–8.CrossRefPubMedPubMedCentralGoogle Scholar
  155. 155.
    Chen H, Sokoll LJ, Udelsman R. Outpatient minimally invasive parathyroidectomy: a combination of sestamibi-SPECT localization, cervical block anesthesia, and intraoperative parathyroid hormone assay. Surgery. 1999;126(6):1016–21. discussion 21–2.CrossRefPubMedPubMedCentralGoogle Scholar
  156. 156.
    Adler JT, Sippel RS, Chen H. The influence of surgical approach on quality of life after parathyroid surgery. Ann Surg Oncol. 2008;15(6):1559–65.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of SurgeryOakland University William Beaumont School of Medicine, Beaumont HospitalsRoyal OakUSA

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