Advertisement
Endocrine| Volume 169, ISSUE 2, P302-310, February 2021

Optimal extent of initial parathyroid resection in patients with multiple endocrine neoplasia syndrome type 1: A meta-analysis

Published:September 29, 2020DOI:https://doi.org/10.1016/j.surg.2020.08.021

      Abstract

      Background

      Hyperparathyroidism is an almost universal feature of multiple endocrine neoplasia type 1 syndrome. We present a systematic review and meta-analysis of the postoperative outcomes of patients undergoing initial operative treatment of primary hyperparathyroidism complicating multiple endocrine neoplasia 1.

      Methods

      A comprehensive literature search was performed with a priori defined exclusion criteria for studies comparing total parathyroidectomy, subtotal parathyroidectomy, and less than subtotal parathyroidectomy.

      Results

      Twenty-one studies incorporating 1,131 patients (272 undergoing total parathyroidectomy, 510 subtotal parathyroidectomy, and 349 less than subtotal parathyroidectomy) were identified. Pooled results revealed increased risk for long-term hypoparathyroidism in total parathyroidectomy patients (relative risk 1.61; 95% confidence interval, 1.12−2.31; P = .009) versus those undergoing subtotal parathyroidectomy. In the less than subtotal parathyroidectomy or subtotal parathyroidectomy comparison group, a greater risk for recurrence of hyperparathyroidism (relative risk 1.37; 95% confidence interval, 1.05−1.79; P = .02), persistence of hyperparathyroidism (relative risk 2.26; 95% confidence interval, 1.49−3.41; P = .0001), and reoperation for hyperparathyroidism (relative risk 2.48; 95% confidence interval, 1.65−3.73; P < .0001) was noted for less than subtotal parathyroidectomy patients, albeit with lesser risk for long-term for hypoparathyroidism (relative risk 0.47; 95% confidence interval, 0.29−0.75; P = .002).

      Conclusion

      Subtotal parathyroidectomy compares favorably to total parathyroidectomy, exhibiting similar recurrence and persistence rates with a decreased propensity for long-term postoperative hypoparathyroidism. The benefit of the decreased risk of hypoparathyroidism in less than subtotal parathyroidectomy is negated by the increase in the risk for recurrence, persistence, and reoperation. Future studies evaluating the performance of less than subtotal parathyroidectomy in specific multiple endocrine neoplasia 1 phenotypes should be pursued in an effort to delineate a patient-tailored, operative approach that optimizes long-term outcomes.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Surgery
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Giusti F.
        • Tonelli F.
        • Brandi M.L.
        Primary hyperparathyroidism in multiple endocrine neoplasia type 1: When to perform surgery?.
        Clinics (Sao Paulo). 2012; 67: 141-144
        • Kamilaris C.D.C.
        • Stratakis C.A.
        Multiple endocrine neoplasia type 1 (MEN1): An update and the significance of early genetic and clinical diagnosis.
        Front Endocrinol (Lausanne). 2019; 10: 339
        • Goudet P.
        • Dalac A.
        • Le Bras M.
        • et al.
        MEN1 disease occurring before 21 years old: A 160-patient cohort study from the Groupe d'etude des Tumeurs Endocrines.
        J Clin Endocrinol Met. 2015; 100: 1568-1577
        • Arnalsteen L.C.
        • Alesina P.F.
        • Quiereux J.L.
        • et al.
        Long-term results of less than total parathyroidectomy for hyperparathyroidism in multiple endocrine neoplasia type 1.
        Surgery. 2002; 132 (discussion 24-25): 1119-1124
        • Thakker R.V.
        • Newey P.J.
        • Walls G.V.
        • et al.
        Clinical practice guidelines for multiple endocrine neoplasia type 1 (MEN1).
        J Clin Endocrinol Met. 2012; 97: 2990-3011
        • Tonelli F.
        • Marini F.
        • Giusti F.
        • Brandi M.L.
        Total and subtotal parathyroidectomy in young patients with multiple endocrine neoplasia type 1-related primary hyperparathyroidism: Potential post-surgical benefits and complications.
        Front Endocrinol (Lausanne). 2018; 9: 558
        • Lamas C.
        • Navarro E.
        • Casterás A.
        • et al.
        MEN1-associated primary hyperparathyroidism in the Spanish registry: Clinical characteristics and surgical outcomes.
        Endocr Connect. 2019; 8: 1416-1424
        • Marini F.
        • Giusti F.
        • Tonelli F.
        • Brandi M.L.
        When parathyroidectomy should be indicated or postponed in adolescents with MEN1-related primary hyperparathyroidism.
        Front Endocrinol (Lausanne). 2018; 9: 597
        • Manoharan J.
        • Albers M.B.
        • Bollmann C.
        • et al.
        Single gland excision for MEN1-associated primary hyperparathyroidism.
        Clini Endocrinol. 2020; 92: 63-70
        • Fyrsten E.
        • Norlen O.
        • Hessman O.
        • Stalberg P.
        • Hellman P.
        Long-term surveillance of treated hyperparathyroidism for multiple endocrine neoplasia type 1: Recurrence or hypoparathyroidism?.
        World J Surg. 2016; 40: 615-621
        • Pieterman C.R.
        • van Hulsteijn L.T.
        • den Heijer M.
        • et al.
        Primary hyperparathyroidism in MEN1 patients: A cohort study with longterm follow-up on preferred surgical procedure and the relation with genotype.
        Ann Surg. 2012; 255: 1171-1178
        • Montenegro FLdM.
        • Brescia M.D.E.G.
        • Lourenço Jr., D.M.
        • et al.
        Could the less-than subtotal parathyroidectomy be an option for treating young patients with multiple endocrine neoplasia type 1-related hyperparathyroidism?.
        Front Endocrinol (Lausanne). 2019; 10: 123
        • Norton J.A.
        • Venzon D.J.
        • Berna M.J.
        • et al.
        Prospective study of surgery for primary hyperparathyroidism (HPT) in multiple endocrine neoplasia-type 1 and Zollinger-Ellison syndrome: Long-term outcome of a more virulent form of HPT.
        Ann Surg. 2008; 247: 501-510
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • Altman D.G.
        • The P.G.
        Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement.
        PLOS Med. 2009; 6e1000097
        • Suurmond R.
        • van Rhee H.
        • Hak T.
        Introduction, comparison, and validation of Meta-Essentials: A free and simple tool for meta-analysis.
        Rese Synth Methods. 2017; 8: 537-553
        • Duval S.
        • Tweedie R.
        A nonparametric “trim and fill” method of accounting for publication bias in meta-analysis.
        J Am Stat Assoc. 2000; 95: 89-98
        • Elaraj D.M.
        • Skarulis M.C.
        • Libutti S.K.
        • et al.
        Results of initial operation for hyperparathyroidism in patients with multiple endocrine neoplasia type 1.
        Surgery. 2003; 134 (discussion 64-65): 858-864
        • Hellman P.
        • Skogseid B.
        • Oberg K.
        • Juhlin C.
        • Akerstrom G.
        • Rastad J.
        Primary and reoperative parathyroid operations in hyperparathyroidism of multiple endocrine neoplasia type 1.
        Surgery. 1998; 124: 993-999
        • Hubbard J.G.
        • Sebag F.
        • Maweja S.
        • Henry J.F.
        Subtotal parathyroidectomy as an adequate treatment for primary hyperparathyroidism in multiple endocrine neoplasia type 1.
        Arch Surg. 2006; 141: 235-259
        • Kluijfhout W.P.
        • Beninato T.
        • Drake F.T.
        • et al.
        Unilateral clearance for primary hyperparathyroidism in selected patients with multiple endocrine neoplasia type 1.
        World J Surg. 2016; 40: 2964-2969
        • Lairmore T.C.
        • Govednik C.M.
        • Quinn C.E.
        • Sigmond B.R.
        • Lee C.Y.
        • Jupiter D.C.
        A randomized, prospective trial of operative treatments for hyperparathyroidism in patients with multiple endocrine neoplasia type 1.
        Surgery. 2014; 156 (discussion 34-5): 1326-1334
        • Lambert L.A.
        • Shapiro S.E.
        • Lee J.E.
        • et al.
        Surgical treatment of hyperparathyroidism in patients with multiple endocrine neoplasia type 1.
        Arch Surg. 2005; 140: 374-382
        • Lee C.H.
        • Tseng L.M.
        • Chen J.Y.
        • Hsiao H.Y.
        • Yang A.H.
        Primary hyperparathyroidism in multiple endocrine neoplasia type 1: Individualized management with low recurrence rates.
        Ann Surg Oncol. 2006; 13: 103-109
        • Malmaeus J.
        • Benson L.
        • Johansson H.
        • et al.
        Parathyroid surgery in the multiple endocrine neoplasia type I syndrome: Choice of surgical procedure.
        World J Surg. 1986; 10: 668-672
        • O'Riordain D.S.
        • O'Brien T.
        • Grant C.S.
        • Weaver A.
        • Gharib H.
        • van Heerden J.A.
        Surgical management of primary hyperparathyroidism in multiple endocrine neoplasia types 1 and 2.
        Surgery. 1993; 114 (discussion 7-9): 1031-1037
        • Schreinemakers J.M.
        • Pieterman C.R.
        • Scholten A.
        • Vriens M.R.
        • Valk G.D.
        • Rinkes I.H.
        The optimal surgical treatment for primary hyperparathyroidism in MEN1 patients: A systematic review.
        World J Surg. 2011; 35: 1993-2005
        • Versnick M.
        • Popadich A.
        • Sidhu S.
        • Sywak M.
        • Robinson B.
        • Delbridge L.
        Minimally invasive parathyroidectomy provides a conservative surgical option for multiple endocrine neoplasia type 1-primary hyperparathyroidism.
        Surgery. 2013; 154: 101-105
        • Waldmann J.
        • Lopez C.L.
        • Langer P.
        • Rothmund M.
        • Bartsch D.K.
        Surgery for multiple endocrine neoplasia type 1-associated primary hyperparathyroidism.
        Br J Surg. 2010; 97: 1528-1534
        • Dotzenrath C.
        • Cupisti K.
        • Goretzki P.E.
        • et al.
        Long-term biochemical results after operative treatment of primary hyperparathyroidism associated with multiple endocrine neoplasia types I and IIa: Is a more or less extended operation essential?.
        Eur J Surg. 2001; 167: 173-178
        • Powell A.C.
        • Alexander H.R.
        • Pingpank J.F.
        • et al.
        The utility of routine transcervical thymectomy for multiple endocrine neoplasia 1-related hyperparathyroidism.
        Surgery. 2008; 144: 878-884
        • Taterra D.
        • Wong L.M.
        • Vikse J.
        • et al.
        The prevalence and anatomy of parathyroid glands: A meta-analysis with implications for parathyroid surgery.
        Langenbecks Arch Surg. 2019; 404: 63-70
        • Salmeron M.D.
        • Gonzalez J.M.
        • Sancho Insenser J.
        • et al.
        Causes and treatment of recurrent hyperparathyroidism after subtotal parathyroidectomy in the presence of multiple endocrine neoplasia 1.
        World J Surg. 2010; 34: 1325-1331
        • Stalberg P.
        • Grodski S.
        • Sidhu S.
        • Sywak M.
        • Delbridge L.
        Cervical thymectomy for intrathymic parathyroid adenomas during minimally invasive parathyroidectomy.
        Surgery. 2007; 141: 626-629
        • Iacobone M.
        • Carnaille B.
        • Palazzo F.F.
        • Vriens M.
        Hereditary hyperparathyroidism: A consensus report of the European Society of Endocrine Surgeons (ESES).
        Langenbecks Arch Surg. 2015; 400: 867-886
        • Naik A.H.
        • Wani M.A.
        • Wani K.A.
        • Laway B.A.
        • Malik A.A.
        • Shah Z.A.
        Intraoperative parathyroid hormone monitoring in guiding adequate parathyroidectomy.
        Indian J Endocrinol Metab. 2018; 22: 410-416
        • Arici C.
        • Cheah W.K.
        • Ituarte P.H.
        • et al.
        Can localization studies be used to direct focused parathyroid operations?.
        Surgery. 2001; 129: 720-729
        • Hughes D.T.
        • Miller B.S.
        • Doherty G.M.
        • Gauger P.G.
        Intraoperative parathyroid hormone monitoring in patients with recognized multiglandular primary hyperparathyroidism.
        World J Surg. 2011; 35: 336-341
        • Alhefdhi A.
        • Ahmad K.
        • Sippel R.
        • Chen H.
        • Schneider D.F.
        Intraoperative parathyroid hormone levels at 5 min can identify multigland disease.
        Ann Surg Oncol. 2017; 24: 733-738
        • Nilubol N.
        • Weisbrod A.B.
        • Weinstein L.S.
        • et al.
        Utility of intraoperative parathyroid hormone monitoring in patients with multiple endocrine neoplasia type 1-associated primary hyperparathyroidism undergoing initial parathyroidectomy.
        World J Surg. 2013; 37: 1966-1972
        • Richards M.L.
        • Thompson G.B.
        • Farley D.R.
        • Grant C.S.
        An optimal algorithm for intraoperative parathyroid hormone monitoring.
        Arch Surg. 2011; 146: 280-285
        • Westerdahl J.
        • Bergenfelz A.
        Parathyroid surgical failures with sufficient decline of intraoperative parathyroid hormone levels: Unobserved multiple endocrine neoplasia as an explanation.
        Arch Surg. 2006; 141: 589-594
        • Keutgen X.M.
        • Nilubol N.
        • Agarwal S.
        • et al.
        Reoperative surgery in patients with multiple endocrine neoplasia type 1 associated primary hyperparathyroidism.
        Ann Surg Oncol. 2016; 23: 701-707
        • Ohe M.N.
        • Santos R.O.
        • Kunii I.S.
        • et al.
        Intraoperative PTH cutoff definition to predict successful parathyroidectomy in secondary and tertiary hyperparathyroidism.
        Braz J Otorhinolaryngol. 2013; 79: 494-499