Skip to main content
Log in

Failure of fragmented parathyroid gland autotransplantation to prevent permanent hypoparathyroidism after total thyroidectomy

  • ORIGINAL ARTICLE
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract

Purpose

Parathyroid autotransplantation during total thyroidectomy leads to higher rates of postoperative hypocalcaemia. It has been argued, however, that it prevents permanent hypoparathyroidism. The impact of autografted normal parathyroid gland fragments on long-term parathyroid status has not been assessed properly. To clarify this, the short- and long-term parathyroid function was assessed in patients with three glands remaining in situ after total thyroidectomy, in whom the fourth gland was either autotransplanted (Tx) or accidentally resected (AR).

Methods

Consecutive patients (n = 669) undergoing first-time total thyroidectomy were prospectively studied recording the number of parathyroid glands remaining in situ: PGRIS =4—(glands autografted + glands in the specimen). The study was focused on the subgroup of 186 patients with three parathyroid glands remaining in situ as a result of either accidental resection (AR, n = 76) or autotransplantation into the sternocleidomastoid muscle (Tx, n = 110). Prevalence of postoperative hypocalcaemia, protracted, and permanent hypoparathyroidism were compared between the two groups. Demographic, disease-related, laboratory, and surgical variables were recorded. All patients were followed for at least 1 year.

Results

Both groups were comparable in terms of disease and extent of surgery. Mean postoperative serum calcium was the same (AR: 1.97 ± 0.2 vs Tx: 1.97 ± 0.22 mmol/L). Rates of protracted (AR: 24% vs Tx: 25.5%) and permanent hypoparathyroidism (AR: 5.3% vs Tx: 7.3%) were similar in both groups.

Conclusions

The prevalence of parathyroid failure syndromes after total thyroidectomy was similar whether a parathyroid gland was inadvertently excised or autotransplanted. Autotransplantation did not influence the permanent hypoparathyroidism rate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Pattou F, Combemale F, Fabre S, Carnaille B, Decoulx M, Wemeau J (1998) Hypocalcaemia following thyroid surgery: incidence and prediction of outcome. World J Surg 22:718–724. doi:10.1007/s002689900459

    Article  CAS  PubMed  Google Scholar 

  2. Bhattacharyya N, Fried MP (2002) Assessment of the morbidity and complications of total thyroidectomy. Arch Otolaryngol Head Neck Surg 128:389–392. doi:10.1001/archotol.128.4.389

    Article  PubMed  Google Scholar 

  3. Abboud B, Sargi Z, Akkam M, Sleilaty F (2002) Risk factors for post-thyroidectomy hypocalcaemia. J Am Coll Surg 195:456–461. doi:10.1016/S1072-7515(02)01310-8

    Article  PubMed  Google Scholar 

  4. Olson JA, DeBenedetti MK, Baumann DS, Wells SA Jr (1996) Parathyroid autotransplantation during thyroidectomy: results of long-term follow-up. Ann Surg 223:472–478

    Article  PubMed  PubMed Central  Google Scholar 

  5. Edafe O, Antakia R, Laskar N, Uttley L, Balasubramanian SP (2014) Systematic review and meta-analysis of predictors of post-thyroidectomy hypocalcaemia. Br J Surg 101:307–320. doi:10.1002/bjs.9384

    Article  CAS  PubMed  Google Scholar 

  6. 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 112:9–14. doi:10.1002/jso.23948

    Article  PubMed  Google Scholar 

  7. Seo ST, Chang JW, Jin J, Lim YC, Rha KS, Koo BS (2015) Transient and permanent hypocalcemia after total thyroidectomy: early predictive factors and long-term follow-up results. Surgery 158:1492–1499. doi:10.1016/j.surg.2015.04.041

    Article  PubMed  Google Scholar 

  8. Bergenfelz A, Jansson S, Kristoffersson A, Mårtensson H, Reihnér E, Wallin G, Lausen I (2008) Complications to thyroid surgery: results as reported in a database from a multicenter audit comprising 3,660 patients. Langenbeck's Arch Surg 393:667–673. doi:10.1007/s00423-008-0366-7

    Article  CAS  Google Scholar 

  9. 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 89:202–217. doi:10.1002/1097-0142(20000701)89:1<202::AID-CNCR27>3.0.CO;2-A

    Article  CAS  PubMed  Google Scholar 

  10. Barczyński M, Cichoń S, Konturek A (2007) Which criterion of intraoperative iPTH assay is the most accurate in prediction of true serum calcium levels after thyroid surgery? Langenbeck's Arch Surg 392:693–698. doi:10.1007/s00423-007-0165-6

    Article  Google Scholar 

  11. Grodski S, Serpell J (2008) Evidence for the role of perioperative PTH measurement after total thyroidectomy as a predictor of hypocalcaemia. World J Surg 32:1367–1373. doi:10.1007/s00268-008-9545-5

    Article  PubMed  Google Scholar 

  12. Paloyan E, Lawrence AM, Paloyan D (1977) Successful autotransplantation of the parathyroid glands during total thyroidectomy for carcinoma. Surg Gynecol Obstetr 145:364–368

    CAS  Google Scholar 

  13. Almquist M, Hallgrimsson P, Nordenström E, Bergenfelz A (2014) Prediction of permanent hypoparathyroidism after total thyroidectomy. World J Surg 38:2613–2620. doi:10.1007/s00268-014-2622-z

    Article  CAS  PubMed  Google Scholar 

  14. Abboud B, Sleilaty G, Zeineddine S, Braidy C, Aouad R, Tohme C, Noun R, Sarkis R (2008) Is therapy with calcium and vitamin D and parathyroid autotransplantation useful in total thyroidectomy for preventing hypocalcemia? Head Neck 30:1148–1154. doi:10.1002/hed.20836

    Article  PubMed  Google Scholar 

  15. Palazzo FF, Sywak MS, Sidhu SB, Barraclough BH, Delbridge LW (2005) Parathyroid autotransplantation during total thyroidectomy—does the number of glands transplanted affect outcome? World J Surg 29:629–631. doi:10.1007/s00268-005-7729-9

    Article  PubMed  Google Scholar 

  16. Zedenius J, Wadstrom C, Delbridge L (1999) Routine autotransplantation of at least one parathyroid gland during total thyroidectomy may reduce permanent hypoparathyroidism to zero. ANZ J Surg 69:794–797. doi:10.1046/j.1440-1622.1999.01697.x

    Article  CAS  Google Scholar 

  17. Lo CY, Lam KY (1999) Parathyroid autotransplantation during thyroidectomy: is frozen section necessary? Arch Surg 134:258–260. doi:10.1001/archsurg.134.3.258

    Article  CAS  PubMed  Google Scholar 

  18. Sitges-Serra A, Ruiz S, Girvent M, Manjón H, Dueñas JP, Sancho JJ (2010) Outcome of protracted hypoparathyroidism after total thyroidectomy. Br J Surg 97:1687–1695

    Article  CAS  PubMed  Google Scholar 

  19. 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 102:359–367. doi:10.1002/bjs.9676

    Article  CAS  PubMed  Google Scholar 

  20. Asari R, Passler C, Kaczirek K, Scheuba C, Niederle B (2008) Hypoparathyroidism after total thyroidectomy: a prospective study. Arch Surg 143:132–137. doi:10.1001/archsurg.2007.55

    Article  CAS  PubMed  Google Scholar 

  21. Lorente-Poch L, Sancho JJ, Muñoz-Nova JL, Sanchez-Velazquez P, Sitges-Serra A (2015) Defining the syndromes of parathyroid failure after total thyroidectomy. Gland Surg 4:82–90. doi:10.3978/j.issn.2227-684X.2014.12.04

    PubMed  PubMed Central  Google Scholar 

  22. Clark OH (1982) Total thyroidectomy: the treatment of choice for patients with differentiated thyroid cancer. Ann Surg 196:361–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Reeve TS, Delbridge L, Cohen A, Crummer P (1987) Total thyroidectomy: the preferred option for multinodular goiter. Ann Surg 206:782–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Al-Dhahri SF, Mubasher M, Mufarji K, Allam OS, Terkawi AS (2014) Factors predicting post-thyroidectomy hypoparathyroidism recovery. World J Surg 38:2304–2310. doi:10.1007/s00268-014-2571-6

    Article  PubMed  Google Scholar 

  25. Attie JN, Khafif RA (1975) Preservation of parathyroid glands during total thyroidectomy: improved technic utilizing microsurgery. Am J Surg 130:399–404. doi:10.1016/0002-9610(75)90472-9

    Article  CAS  PubMed  Google Scholar 

  26. Ohman U, Granberg PO, Lindell B (1978) Function of the parathyroid glands after total thyroidectomy. Surg Gynecol Obstetr 146:773–778

    CAS  Google Scholar 

  27. Wells SA Jr, Ellis GJ, Gunnells JC, Schneider AB, Sherwood LM (1976) Parathyroid autotransplantation in primary parathyroid hyperplasia. N Engl J Med 295:57–62. doi:10.1056/NEJM197607082950201

    Article  PubMed  Google Scholar 

  28. Paloyan E, Lawrence AM, Brooks MH, Pickleman JR (1976) Total thyroidectomy and parathyroid autotransplantation for radiation-associated thyroid cancer. Surgery 80:70–76

    CAS  PubMed  Google Scholar 

  29. Salander H, Tisell LE (1977) Incidence of hypoparathyroidism after radical surgery for thyroid carcinoma and autotransplantation of parathyroid glands. Am J Surg 134:358–362. doi:10.1016/0002-9610(77)90406-8

    Article  CAS  PubMed  Google Scholar 

  30. 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 262:641–646. doi:10.1097/SLA.0000000000001464

    Article  PubMed  PubMed Central  Google Scholar 

  31. Prichard RS, Edhouse PJ, Sidhu SB, Sywak MS, Delbridge L (2011) Postoperative partial hypoparathyroidism: an under-recognized disorder. ANZ J Surg 81:524–527. doi:10.1111/j.1445-2197.2010.05633.x

    Article  PubMed  Google Scholar 

  32. Paek SH, Lee YM, Min SY, Kim SW, Chung KW, Youn YK (2013) Risk factors of hypoparathyroidism following total thyroidectomy for thyroid cancer. World J Surg 37:94–101. doi:10.1007/s00268-012-1809-4

    Article  PubMed  Google Scholar 

  33. Ahmed N, Aurangzeb M, Muslim M, Zarin M (2013) Routine parathyroid autotransplantation during total thyroidectomy: a procedure with predictable outcome. J Pak Med Assoc 63:190–193

    PubMed  Google Scholar 

  34. Hallgrimsson P, Nordenstrom E, Almquist M, Bergenfelz AO (2012) Risk factors for medically treated hypocalcaemia after surgery for Graves' disease: a Swedish multicenter study of 1,157 patients. World J Surg 36:1933–1942. doi:10.1007/s00268-012-1574-4

    Article  CAS  PubMed  Google Scholar 

  35. Sakorafas GH, Stafyla V, Bramis C, Kotsifopoulos N, Kolettis T, Kassaras G (2005) Incidental parathyroidectomy during thyroid surgery: an underappreciated complication of thyroidectomy. World J Surg 29:1539–1544. doi:10.1007/s00268-005-0032-y

    Article  PubMed  Google Scholar 

  36. Sheahan P, Mehanna R, Basheeth N, Murphy MS (2013) Is systematic identification of all four parathyroid glands necessary during total thyroidectomy?: a prospective study. Laryngoscope 123:2324–2328. doi:10.1002/lary.23954

    Article  CAS  PubMed  Google Scholar 

  37. Conti-Freitas LC, Foss-Freitas MC, Lucca LJ, da Costa JAC, Mamede RCM, Foss MC (2009) Dynamics of parathyroid hormone secretion after total parathyroidectomy and autotransplantation. World J Surg 33:1403–1407. doi:10.1007/s00268-009-0057-8

    Article  PubMed  Google Scholar 

  38. El-Sharaky MI, Kahalil MR, Sharaky O, Sakr MF, Fadaly GA, El-Hammadi HA, Moussa M (2003) Assessment of parathyroid autotransplantation for preservation of parathyroid function after total thyroidectomy. Head Neck 25:799–807. doi:10.1002/hed.10278

    Article  PubMed  Google Scholar 

  39. Lo CY, Tam SC (2001) Parathyroid autotransplantation during thyroidectomy: documentation of graft function. Arch Surg 136:1381–1385. doi:10.1001/archsurg.136.12.1381

    Article  CAS  PubMed  Google Scholar 

  40. Cavallaro G, Iorio O, Centanni M, Porta N, Iossa A, Gargano L, Del Duca S, Gurrado A, Testini M, Petrozza V, Silecchia V (2015) Parathyroid reimplantation in forearm subcutaneous tissue during thyroidectomy: a simple and effective way to avoid hypoparathyroidism. World J Surg 39:1936–1942. doi:10.1007/s00268-015-3070-0

    Article  PubMed  Google Scholar 

  41. 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)

    Google Scholar 

  42. Sitges-Serra A, Gallego-Otaegui L, Suárez S, Lorente-Poch L, Munné A, Sancho JJ (2016) Inadvertent parathyroidectomy during total thyroidectomy and central neck dissection for papillary thyroid carcinoma. Surgery. doi:10.1016/j.surg.2016.08.021

    PubMed  Google Scholar 

Download references

Acknowledgements

No sources of funding for the work have been reported.

Authors’ contributions

(1) Conception and design: Leyre Lorente-Poch, MD, Juan José Sancho, MD, and Antonio Sitges-Serra, MD, FRCS; (2) administrative support: none; (3) provision of study materials or patients: Leyre Lorente-Poch, MD, Carlos Martínez-Ruiz, MD, Lander Gallego-Otaegui; (4) collection and assembly of data: Leyre Lorente-Poch, MD, Carlos Martínez-Ruiz, MD, Lander Gallego-Otaegui; (5) data analysis and interpretation: Juan José Sancho, MD, Antonio Sitges-Serra, MD, FRCS; (6) manuscript writing: Leyre Lorente-Poch, MD, Juan José Sancho, MD, Jose Luis Muñoz, MD, and Antonio Sitges-Serra, MD, FRCS; (7) final approval of manuscript: all authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antonio Sitges-Serra.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical considerations

The authors of the present study state that the protocol for the research project has been approved by a suitably constituted Ethics Committee of the Hospital del Mar within which the work was undertaken and that it conforms to the provisions of in accordance with the Helsinki Declaration as revised in 2013. The study outcomes will affect the future management of our patients since the use of parathyroid autotransplantation will become restrictive.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lorente-Poch, L., Sancho, J., Muñoz, J.L. et al. Failure of fragmented parathyroid gland autotransplantation to prevent permanent hypoparathyroidism after total thyroidectomy. Langenbecks Arch Surg 402, 281–287 (2017). https://doi.org/10.1007/s00423-016-1548-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-016-1548-3

Keywords

Navigation