Abstract
Background
Careful parathyroid gland dissection and in situ preservation was the time-honored approach to prevent parathyroid failure after total thyroidectomy. The relative success of parathyroid autotransplantation of hyperplastic parathyroid tissue in patients with renal or hereditary hyperparathyroidism did popularize the use of normal parathyroid tissue autografts during thyroidectomy to prevent permanent hypoparathyroidism. Proof of autograft function in this setting, however, is controversial.
Purpose
This narrative review aims at reviewing critically the current status of parathyroid autotransplantation during total thyroidectomy. It is also meant to analyze from the historical, methodological, and clinical points of view the claimed benefit of normal parathyroid gland autotransplantation. A focus is placed on the prevention of permanent hypoparathyroidism by parathyroid autotransplantation.
Conclusions
Liberal parathyroid autotransplantation was proposed in the mid 1970s but evidence of function is scarce. Proofs are accumulating that parathyroid autografts not only increase the rate of postoperative hypocalcemia, but may be also contribute to permanent hypoparathyroidism.
Similar content being viewed by others
References
Duclos A, Peix JL, Colin C, Kraimps JL, Menegaux F, Pattou F, Sebag F, Touzet S, Bourdy S, Voirin N, Lifante JC, CATHY Study Group (2012) Influence of experience on performance of individual surgeons in thyroid surgery: prospective cross sectional multicentre study. BMJ 344(jan10 2):d8041. https://doi.org/10.1136/bmj.d8041
Hundahl SA, Cady B, Cunningham MP, Mazzaferri E, McKee RF, Rosai J, Shah JP, Fremgen AM, Stewart AK, Hölzer S (2000) Initial results from a prospective cohort study of 5583 cases of thyroid carcinoma treated in the United States during 1996. U.S. and German Thyroid Cancer Study Group. An American College of Surgeons Commission on Cancer Patient Care Evaluation study. Cancer 89(1):202–217. https://doi.org/10.1002/1097-0142(20000701)89:1<202::AID-CNCR27>3.0.CO;2-A
Vrachimis A, Wenning C, Gerß J, Dralle H, Vaez Tabassi M, Schober O, Riemann B, MSDS study group (2015) Not all DTC patients with N positive disease deserve the attribution “high risk”. Contribution of the MSDS trial. J Surg Oncol 112(1):9–14. https://doi.org/10.1002/jso.23948
Nawrot I, Pragacz A, Pragacz K, Grzesiuk W, Barczyński M (2014) Total thyroidectomy is associated with increased prevalence of permanent hypoparathyroidism. Med Sci Monit 20:1675–1681. https://doi.org/10.12659/MSM.890988
Viola D, Materazzi G, Valerio L, Molinaro E, Agate L, Faviana P, Seccia V, Sensi E, Romei C, Piaggi P, Torregrossa L, Sellari-Franceschini S, Basolo F, Vitti P, Elisei R, Miccoli P (2015) Randomized, prospective trial finds no clinical advantage to prophylactic central-neck dissection for papillary thyroid cancer. J Clin Endocrinol Metab 100(4):1316–1324. https://doi.org/10.1210/jc.2014-3825
Lorente-Poch L, Sancho JJ, Ruiz S, Sitges-Serra A (2015) Importance of in situ preservation of parathyroid glands during total thyroidectomy. Br J Surg 102(4):359–367. https://doi.org/10.1002/bjs.9676
Thompson NW, Olsen WR, Hoffman GL (1973) The continuing development of the technique of thyroidectomy. Surgery 73(6):913–927
Proye C, Maes B, Bondil P, Vanseymortier L, Lagache G (1982) Parathyroid risk in thyroid surgery (in French). J Chir 119(8–9):491–498
Sitges-Serra A, Gallego-Otaegui L, Suárez S, Lorente-Poch L, Munné A, Sancho JJ (2017) Inadvertent parathyroidectomy during total thyroidectomy and central neck dissection for papillary thyroid carcinoma. Surgery 161(3):712–719. https://doi.org/10.1016/j.surg.2016.08.021
Ondik MP, McGinn J, Ruggiero F, Kim SW, Chung KW, Youn YK (2009) Unintentional parathyroidectomy and hypoparathyroidism in secondary central compartment surgery for thyroid cancer. Head Neck 32:462–466
Applewhite MK, White MG, Xiong M, Pasternak JD, Abdulrasool L, Ogawa L, Suh I, Gosnell JE, Kaplan EL, Duh QY, Angelos P, Shen WT, Grogan RH (2016) Incidence, risk factors, and clinical outcomes of incidental parathyroidectomy during thyroid surgery. Ann Surg Oncol 23(13):4310–4315. https://doi.org/10.1245/s10434-016-5439-1
Lahey FH (1926) Transplantation of the parathyroids in partial thyroidectomy. Surg Gynecol Obstet 62:508–509
Alveryd A (1968) Parathyroid glands in thyroid surgery I. Anatomy of parathyroid glands. II. Postoperative hypoparathyroidism—identification and autotransplantation of parathyroid glands. Acta Chir Scand 389:1–120
Wells SA, Ellis GJ, Gunnells JC, Schneider AB, Sherwood LM (1976) Parathyroid autotransplantation in primary parathyroid hyperplasia. N Engl J Med 295(2):57–62. https://doi.org/10.1056/NEJM197607082950201
Wells SA, Gunnells JC, Shelburne JD, Schneider AB, Sherwood LM (1975) Transplantation of the parathyroid glands in man: clinical indications and results. Surgery 78(1):34–44
Paloyan E, Lawrence AM, Paloyan D (1977) Successful autotransplantation of the parathyroid glands during total thyroidectomy for carcinoma. Surg Gynecol Obstet 145:364–368
Olson JA Jr, DeBenedetii MK, Baumann DS, Wells SA Jr (1996) Parathyroid autotransplantation during thyroidectomy. Ann Surg 223(5):472–480. https://doi.org/10.1097/00000658-199605000-00003
Zedenius J, Wadstrom C, Delbridge L (1999) Routine autotransplantation of at least one parathyroid gland during total thyroidectomy may reduce permanent hypoparathyroidism to zero. Aust N Z J Surg 69(11):794–797. https://doi.org/10.1046/j.1440-1622.1999.01697.x
Lo CY, Lam KY (2001) Routine parathyroid autotransplantation during thyroidectomy. Surgery 129(3):318–323. https://doi.org/10.1067/msy.2001.111125
Moley JF, Skinner M, Gillanders WE, Lairmore TC, Rowland KJ, Traugott AL, Jin LX, Wells SA Jr (2015) Management of the parathyroid glands during preventive thyroidectomy in patients with multiple endocrine neoplasia type 2. Ann Surg 262(4):641–646. https://doi.org/10.1097/SLA.0000000000001464
Prichard RS, Edhouse PJ, Sidhu SB, Sywak MS, Delbridge L (2011) Post-operative partial hypoparathyroidism: an under-recognized disorder. ANZ J Surg 81(7–8):524–527. https://doi.org/10.1111/j.1445-2197.2010.05633.x
Lang BH, Chan DT, Chow FC (2016) Visualizing fewer parathyroid glands may be associated with lower hypoparathyroidism following total thyroidectomy. Langenbeck’s Arch Surg 401(2):231–238. https://doi.org/10.1007/s00423-016-1386-3
Pattou F, Combemale F, Fabre S, Carnaille B, Decoulx M, Wemeau JL, Racadot A, Proye C (1998) Hypocalcemia following thyroid surgery: incidence and prediction of outcome. World J Surg 22(7):718–724. https://doi.org/10.1007/s002689900459
Sitges-Serra A, Ruiz S, Girvent M, Manjón H, Dueñas JP, Sancho JJ (2010) Outcome of protracted hypoparathyroidism after total thyroidectomy. Br J Surg 97(11):1687–1695. https://doi.org/10.1002/bjs.7219
Lorente-Poch L, Sancho JJ, Muñoz-Nova JL, Sánchez-Velázquez P, Sitges-Serra A (2015) Defining the syndromes of parathyroid failure after total thyroidectomy. Gland Surg 4(1):82–90. https://doi.org/10.3978/j.issn.2227-684X.2014.12.04
Lorente-Poch L, Sancho J, Muñoz JL, Gallego-Otaegui L, Martínez-Ruiz C, Sitges-Serra A (2017) Failure of fragmented parathyroid gland autotransplantation to prevent permanent hypoparathyroidism after total thyroidectomy. Langenbeck's Arch Surg 402(2):281–287. https://doi.org/10.1007/s00423-016-1548-3
Lo CY, Lam KY, Weber CJ, Shaha AR, Davis O (1998) Postoperative hypocalcemia in patients who did or did not undergo parathyroid autotransplantation during thyroidectomy: a comparative study. Surgery 124(6):1081–1087. https://doi.org/10.1067/msy.1998.92560
Funahashi H, Satoh Y, Imai T, Ohno M, Narita T, Katoh M, Tanaka Y, Andoh H, Miyazaki K (1993) Our technique of parathyroid autotransplantation in operation for papillary thyroid carcinoma. Surgery 114(1):92–96
Kikumori T, Imai T, Tanaka Y, Oiwa M, Mase T, Funahashi H (1999) Parathyroid autotransplantation with total thyroidectomy for thyroid carcinoma: long-term follow-up of grafted parathyroid function. Surgery 125(5):504–508. https://doi.org/10.1016/S0039-6060(99)70201-1
Lo CY, Tam SC (2001) Parathyroid autotransplantation during thyroidectomy: documentation of graft function. Arch Surg 136(12):1381–1385. https://doi.org/10.1001/archsurg.136.12.1381
El-Sharaky MI, Kahalil MR, Sharaky O, Sakr MF, Fadaly GA, El-Hammadi H, Moussa MM (2003) Assessment of parathyroid autotransplantation for preservation of parathyroid function after total thyroidectomy. Head Neck 25(10):799–807. https://doi.org/10.1002/hed.10278
Sierra M, Herrera MF, Herrero B, Jiménez F, Sepúlveda J, Lozano RR, Gamino R, González O, Correa-Rotter R (1998) Prospective biochemical and scintigraphic evaluation of autografted normal parathyroid glands in patients undergoing thyroid operations. Surgery 124(6):1005–1011. https://doi.org/10.1067/msy.1998.92003
Cavallaro G, Iorio O, Centanni M, Porta N, Iossa A, Gargano L, Del Duca S, Gurrado A, Testini M, Petrozza V, Silecchia G (2015) Parathyroid reimplantation in forearm subcutaneous tissue during thyroidectomy: a simple and effective way to avoid hypoparathyroidism. World J Surg 39(8):1936–1942. https://doi.org/10.1007/s00268-015-3070-0
Casanova D, Sarfati E, De Francisco A, Amado JA, Arias M, Dubost C (1991) Secondary hyperparathyroidism: diagnosis of site of recurrence. World J Surg 15(4):546–549. https://doi.org/10.1007/BF01675660
Lorente L, Sancho JJ, Sitges-Serra A (2015) European survey of the indications and technique of parathyroid autotransplantation during thyroidectomy. Langenbeck’s Arch Surg 400:396 (Abstract)
Gauger P, Reeve TS, Wilkinson M, Delbridge LW (2000) Routine parathyroid autotransplantation during total thyroidectomy: the influence of technique. Eur J Surg 166(8):605–609. https://doi.org/10.1080/110241500750008240
Promberger R, Ott J, Kober F, Mikola B, Karik M, Freissmuth M, Hermann M (2010) Intra- and postoperative parathyroid hormone-kinetics do not advocate for autotransplantation of discolored parathyroid glands during thyroidectomy. Thyroid 20(12):1371–1375. https://doi.org/10.1089/thy.2010.0157
Lang BH, Chan DT, Chow FC, Wong KP, Chang RY (2016) The association of discolored parathyroid glands and hypoparathyroidism following total thyroidectomy. World J Surg 40(7):1611–1617. https://doi.org/10.1007/s00268-016-3462-9
Vidal Fortuny J, Belfontali V, Sadowski SM, Karenovics W, Guigard S, Triponez F (2016) Parathyroid gland angiography with indocyanine green fluorescence to predict parathyroid function after thyroid surgery. Br J Surg 103(5):537–543. https://doi.org/10.1002/bjs.10101
Villarroya-Marquina I, Sancho J, Lorente-Poch L, Gallego-Otaegui L, Sitges-Serra A (2018) Time to parathyroid function recovery in patients with protracted hypoparathyroidism after total thyroidectomy. Eur J Endocrinol 178(1):105–113. https://doi.org/10.1530/EJE-17-0589
Lang BH, Wong CK, Hung HT, Wong KP, Mak KL, Au KB (2017) Indocyanine green fluorescence angiography for quantitative evaluation of in situ parathyroid gland perfusion and function after total thyroidectomy. Surgery 161(1):87–95. https://doi.org/10.1016/j.surg.2016.03.037
Savarise M, Senkowski C (eds) (2017) Principles of coding and reimbursement for surgeons. Springer International Publishing, Switzerland, pp 330–331
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants performed by any of the authors.
Rights and permissions
About this article
Cite this article
Sitges-Serra, A., Lorente-Poch, L. & Sancho, J. Parathyroid autotransplantation in thyroid surgery. Langenbecks Arch Surg 403, 309–315 (2018). https://doi.org/10.1007/s00423-018-1654-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00423-018-1654-5