Abstract
Background
Parathyroidectomy is the only definitive treatment for primary hyperparathyroidism (PHPT). Precise localization of abnormal glands is a key to a successful surgery. Most patients are expected to be successfully treated with focused parathyroidectomy. However, this approach is associated with a risk of existing multiglandular disease which may lead to the postoperative persistence of PHPT.
Methods
Eight hundred ten patients who underwent an initial surgery for PHPT at SPBU Hospital in 2017–2018 were included in the study. Preoperative imaging results were evaluated. Multivariate logistic regressions were calculated to estimate predictive values of preoperative data for the risk of postoperative persistence and risk of MGD.
Results
Multiglandular disease was found to be a leading cause of persistent hyperparathyroidism. An anamnesis of thyroid surgery was found to be a significant risk factor for the persistence of hyperparathyroidism. The rate of persistence did not differ significantly between groups with bilateral neck exploration and focused parathyroidectomy. Age, sex, body mass index as well as negative results of preoperative US, MIBI, and 4D CT were not independently associated with a higher risk of MGD. All preoperative imaging modalities showed from low to moderate sensitivity for the detection of MGD. The frequency of cases of a missed second adenoma did not differ significantly between patients with concordant and discordant preoperative data. There were 7 cases with previously unsuspected second adenomas found solely due to bilateral neck exploration.
Conclusions
None of the combination of preoperative visualization modalities was able to rule out the MGD and reliably identify patients for focused parathyroidectomy. Additional preoperative visualization failed to improve overall results. Bilateral neck exploration appeared to have a slight benefit for the patients with concordant preoperative imaging results.
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References
Nilsson IL (2019) Primary hyperparathyroidism: should surgery be performed on all patients? Current evidence and residual uncertainties. J Intern Med 285:149–164. https://doi.org/10.1111/joim.12840
Zanocco K, Heller M, Sturgeon C (2011) Cost-effectiveness of parathyroidectomy for primary hyperparathyroidism. Endocr Pract 17:69–74. https://doi.org/10.4158/EP10311.RA
Coakley AJ, Kettle AG, Wells CP et al (1989) 99Tcm sestamibi–a new agent for parathyroid imaging. Nucl Med Commun 10(11):791–794
Johnson NA, Tublin ME, Ogilvie JB (2007) Parathyroid imaging: technique and role in the preoperative evaluation of primary hyperparathyroidism. Am J Roentgenol 188:1706–1715. https://doi.org/10.2214/AJR.06.0938
Kelly HR, Hamberg LM, Hunter GJ (2014) 4D-CT for preoperative localization of abnormal parathyroid glands in patients with hyperparathyroidism: accuracy and ability to stratify patients by unilateral versus bilateral disease in surgery-naïve and re-exploration patients. Am J Neuroradiol 35:176–181. https://doi.org/10.3174/ajnr.A3615
Starker LF, Mahajan A, Björklund P et al (2011) 4D parathyroid CT as the initial localization study for patients with de novo primary hyperparathyroidism. Ann Surg Oncol 18:1723–1728. https://doi.org/10.1245/s10434-010-1507-0
Day KM, Elsayed M, Beland MD, Monchik JM (2015) The utility of 4-dimensional computed tomography for preoperative localization of primary hyperparathyroidism in patients not localized by sestamibi or ultrasonography. Surgery 157:534–539. https://doi.org/10.1016/j.surg.2014.11.010
Orevi M, Freedman N, Mishani E et al (2014) Localization of parathyroid adenoma by 11C-choline PET/CT. Clin Nucl Med 39:1033–1038. https://doi.org/10.1097/rlu.0000000000000607
Tay D, Das JP, Yeh R (2021) Preoperative localization for primary hyperparathyroidism: a clinical review. Biomedicines 9:390. https://doi.org/10.3390/biomedicines9040390
Barczyński M, Bränström R, Dionigi G, Mihai R (2015) Sporadic multiple parathyroid gland disease—a consensus report of the European Society of Endocrine Surgeons (ESES). Langenbeck’s Arch Surg 400:887–905. https://doi.org/10.1007/s00423-015-1348-1
Shah US, Mccoy KL, Kelley ML et al (2022) How and when is multiglandular disease diagnosed in sporadic primary hyperparathyroidism? Surgery 171(1):35–39. https://doi.org/10.1016/j.surg.2021.09.018
Thier M, Daudi S, Bergenfelz A, Almquist M (2018) Predictors of multiglandular disease in primary hyperparathyroidism. Langenbeck’s Arch Surg 403:103–109. https://doi.org/10.1007/s00423-017-1647-9
Kebebew E (2006) Predictors of single-gland vs multigland parathyroid disease in primary hyperparathyroidism. Arch Surg 141:777. https://doi.org/10.1001/archsurg.141.8.777
Mazeh H, Chen H, Leverson G, Sippel RS (2013) Creation of a “Wisconsin Index” nomogram to predict the likelihood of additional hyperfunctioning parathyroid glands during parathyroidectomy. Ann Surg 257:138–141. https://doi.org/10.1097/SLA.0b013e31825ffbe1
Serradilla-Martín M, Palomares-Cano A, Cantalejo-Díaz M et al (2021) Usefulness of the Wisconsin and CaPTHUS indices for predicting multiglandular disease in patients with primary hyperparathyroidism in a southern European population. Gland Surg 10:861–869. https://doi.org/10.21037/gs-20-857
De Pasquale L, Lori E, Bulfamante AM et al (2021) Evaluation of Wisconsin and CaPTHUS indices usefulness for predicting monoglandular and multiglandular disease in patients with primary hyperparathyroidism through the analysis of a single-center experience. Int J Endocrinol 2040284:1–8. https://doi.org/10.1155/2021/2040284
Dobrinja C, Santandrea G, Giacca M et al (2017) Effectiveness of intraoperative parathyroid monitoring (ioPTH) in predicting a multiglandular or malignant parathyroid disease. Int J Surg 41:26–33. https://doi.org/10.1016/j.ijsu.2017.02.063
Morris LF, Zanocco K, Ituarte PHG et al (2010) The value of intraoperative parathyroid hormone monitoring in localized primary hyperparathyroidism: a cost analysis. Ann Surg Oncol 17:679–685. https://doi.org/10.1245/s10434-009-0773-1
Barczyński M, Gołkowski F, Nawrot I (2015) The current status of intraoperative iPTH assay in surgery for primary hyperparathyroidism. Gland Surg 4(1):36–43. https://doi.org/10.3978/j.issn.2227-684X.2015.01.01
Badii B, Staderini F, Foppa C et al (2017) Cost-benefit analysis of the intraoperative parathyroid hormone assay in primary hyperparathyroidism. Head Neck 39:241–246. https://doi.org/10.1002/hed.24567
Haciyanli M, Lal G, Morita E et al (2003) Accuracy of preoperative localization studies and intraoperative parathyroid hormone assay in patients with primary hyperparathyroidism and double adenoma. J Am Coll Surg 197:739–746. https://doi.org/10.1016/S1072-7515(03)00676-8
Sugg SL, Krzywda EA, Demeure MJ, Wilson SD (2004) Detection of multiple gland primary hyperparathyroidism in the era of minimally invasive parathyroidectomy. Surgery 136:1303–1309. https://doi.org/10.1016/j.surg.2004.06.062
Sleptsov IV, Vybornova NB, Chernikov RA, et al (2015) Modified quick parathyroid hormone test in surgery of primary hyperparathyroidism. Endocr Surg 9(4):12–21. (In Russ.) https://doi.org/10.14341/serg201541221
Ahmadieh H, Kreidieh O, Akl EA, El-Hajj Fuleihan G (2020) Minimally invasive parathyroidectomy guided by intraoperative parathyroid hormone monitoring (IOPTH) and preoperative imaging versus bilateral neck exploration for primary hyperparathyroidism in adults. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD010787.pub2
Sleptsov IV, Chernikov RA, Bubnov AN et al (2012) Minimally invasive surgery of primary hyperparathyroidism. Endocrine Surgery 6:24–33 (In Russ.)
Fazendin JM, Lindeman B, Chen H (2020) Preoperative parathyroid localization does not improve surgical outcomes for patients with primary hyperparathyroidism. Am J Surg 220(3):533–535. https://doi.org/10.1016/j.amjsurg.2020.04.029
Norman J, Lopez J, Politz D (2012) Abandoning unilateral parathyroidectomy: why we reversed our position after 15,000 parathyroid operations. J Am Coll Surg 214:260–269. https://doi.org/10.1016/j.jamcollsurg.2011.12.007
Walsh NJ, Sullivan BT, Duke WS, Terris DJ (2019) Routine bilateral neck exploration and four-gland dissection remains unnecessary in modern parathyroid surgery. Laryngoscope Investig Otolaryngo 4:188–192. https://doi.org/10.1002/lio2.223
Norlén O, Wang KC, Tay YK et al (2015) No need to abandon focused parathyroidectomy. Ann Surg 261:991–996. https://doi.org/10.1097/SLA.0000000000000715
Jinih M, O’connell E, O’leary DP et al (2017) Focused versus bilateral parathyroid exploration for primary hyperparathyroidism: a systematic review and meta-analysis. Ann Surg Oncol. 24(7):1924–1934. https://doi.org/10.1245/S10434-016-5694-1
Dy BM, Richards ML, Vazquez BJ et al (2012) Primary hyperparathyroidism and negative Tc99 sestamibi imaging: to operate or not? Ann Surg Oncol 19:2272–2278. https://doi.org/10.1245/s10434-012-2325-3
Elaraj DM (2010) Are Additional localization studies and referral indicated for patients with primary hyperparathyroidism who have negative sestamibi scan results? Arch Surg 145:578. https://doi.org/10.1001/archsurg.2010.108
Wachtel H, Bartlett EK, Kelz RR et al (2014) Primary hyperparathyroidism with negative imaging. Ann Surg 260:474–482. https://doi.org/10.1097/SLA.0000000000000875
Ellika S, Patel S, Aho T, Marin H (2013) Preoperative localization of parathyroid adenomas using 4-dimensional computed tomography: a pictorial essay. Can Assoc Radiol J 64:258–268. https://doi.org/10.1016/j.carj.2012.03.002
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Study conception and design: Dmitrii M. Buzanakov, Ilya V. Sleptsov, Roman A. Chernikov, Arseny A. Semenov. Surgeons: Ilya V. Sleptsov, Roman A. Chernikov, Arseny A. Semenov, Konstantin Y. Novokshonov, Julia V. Karelina, Viktor A. Makarin, Anna A. Uspenskaya, Natalya I. Timofeeva, Igor K. Chinchuk, Elisey A. Fedorov, Natalya A. Gorskaya, Ilya V. Sablin, Yuriy N. Malugov, Svetlana A. Alekseeva. Acquisition of data: Svetlana A. Alekseeva, Alexander A. Pushkaruk, Ksenya A. Gerasimova, Shamil S. Shikhmagomedov, Mikhail.V. Lyubimov, Dina.V. Rebrova. Data analysis: Dmitrii M. Buzanakov, Timur A. Dzhumatov, Anna V. Zolotoukho. Writing — original draft preparation: Dmitrii M. Buzanakov, Anna V. Zolotoukho. Writing — review and editing: Ilya V. Sleptsov, Roman A. Chernikov, Arseny A. Semenov, Anna V. Zolotoukho. Supervision: Alexander N. Bubnov.
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Buzanakov, D.M., Sleptsov, I.V., Semenov, A.A. et al. Persistence of primary hyperparathyroidism: a single-center experience. Langenbecks Arch Surg 407, 3651–3659 (2022). https://doi.org/10.1007/s00423-022-02711-5
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DOI: https://doi.org/10.1007/s00423-022-02711-5