Skip to main content

Advertisement

SpringerLink
Log in

Prevalence and risk factors for hypoparathyroidism following total thyroidectomy in Spain: a multicentric and nation-wide retrospective analysis

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

A Correction to this article was published on 22 October 2019

This article has been updated

Abstract

Purpose

The prevalence of postoperative hypoparathyroidism has been studied in registries and in surgical series with highly variable and imprecise results. However, the frequency of this hormonal deficiency in the clinical practice of endocrinologists is not known with accuracy. We aimed to assess the prevalence and risk factors of hypoparathyroidism in patients undergoing total thyroidectomy in Spain.

Methods

We designed a retrospective, multicentre and nation-wide protocol including all patients with total thyroidectomy who were seen in the endocrinology clinic of the participant centers from January to March 2018. Prevalence of hypoparathyroidism was evaluated at discharge of surgery, 3–6 months after surgery, 12 months after surgery and at last visit. Twenty hospitals participated in the study.

Results

Of 1792 patients undergoing total thyroidectomy, 866 (48.3%) developed postoperative hypoparathyroidism at discharge of surgery. Most of them recover parathyroid function over time. Prevalence of hypoparathyroidism at 3–6 months, 12 months and at last visit was 22.9%, 16.7% and 14.5%, respectively. The risk of developing definitive hypoparathyroidism was related to the presence of parathyroid tissue at histology, lymph node dissection, and two-stage thyroidectomy. Patients with thyroid cancer, with higher postoperative calcium levels and treated by expert surgical teams exhibited lower risk of developing permanent hypoparathyroidism.

Conclusions

Although most patients with postsurgical hypoparathyroidism recover parathyroid function, the prevalence of permanent disease in clinical practice is non negligible (14.5%). Postoperative calcium, extent and timing of surgery, the presence of cancer, expert surgical team, and parathyroid tissue at histology are predictors of permanent hypoparathyroidism.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Change history

  • 22 October 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

References

  1. J. Bollerslev, L. Rejnmark, C. Marcocci, D.M. Shoback, A. Sitges-Serra, W. van Biesen, O.M. Dekkers, European Society of Endocrinology, European society of endocrinology clinical guideline: treatment of chronic hypoparathyroidism in adults. Eur. J. Endocrinol. 173, G1–G20 (2015)

    CAS  PubMed  Google Scholar 

  2. M.L. Brandi, J.P. Bilezikian, D. Shoback, R. Bouillon, B.L. Clarke, R.V. Thakker, A.A. Khan, J.T. Potts Jr., Management of hypoparathyroidism: Summary statement and guidelines. J. Clin. Endocrinol. Metab. 101, 2273–2283 (2016)

    CAS  PubMed  Google Scholar 

  3. B.L. Clarke, E.M. Brown, M.T. Collins, H. Jüppner, P. Lakatos, M.A. Levine, M.M. Mannstadt, J.P. Bilezikian, A.F. Romanischen, R.V. Thakker, Epidemiology and diagnosis of hypoparathyroidism. J. Clin. Endocrinol. Metab. 101, 2284–2299 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  4. B.L. Clarke, C. Leibson, J. Emerson, J.E. Ransom, H. Lagast, Co-morbid medical conditions associated with prevalent hypoparathyroidism: a population-based study (abstract SA0170). J. Bone Min. Res. 26, S182 (2011)

    Google Scholar 

  5. L. Underbjerg, T. Sikjaer, L. Mosekilde, L. Rejnmark, Cardiovascular and renal complications to postsurgical hypoparathyroidism: a Danish nationwide controlled historic follow-up study. J. Bone Miner. Res. 28, 2277–2285 (2013)

    PubMed  Google Scholar 

  6. L. Underbjerg, T. Sikjaer, L. Mosekilde, L. Rejnmark, The epidemiology of nonsurgical hypoparathyroidism in Denmark: A nationwide case finding study. J. Bone Miner. Res. 30, 1738–1744 (2015)

    CAS  PubMed  Google Scholar 

  7. B.C. Stack Jr, D.N. Bimston, D.L. Bodenner, E.M. Brett, H. Dralle, L.A. Orloff, J. Pallota, S.K. Snyder, R.J. Wong, G.W. Randolph, American Association of Clinical Endocrinologists and American College of Endocrinology disease state clinical review: postoperative hypoparathyroidism - Definitions and management. Endocr. Pract. 21, 674–685 (2015)

    PubMed  Google Scholar 

  8. P. Iglesias, J.J. Díez, Endocrine complications of surgical treatment of thyroid cancer: an update. Exp. Clin. Endocrinol. Diabetes 125, 497–505 (2017)

    CAS  PubMed  Google Scholar 

  9. Y.S. Lee, K.H. Nam, W.Y. Chung, H.S. Chang, C.S. Park, Postoperative complications of thyroid cancer in a single center experience. J. Korean Med. Sci. 25, 541–545 (2010)

    PubMed  PubMed Central  Google Scholar 

  10. L. Youngwirth, J. Benavidez, R. Sippel, H. Chen, Parathyroid hormone deficiency after total thyroidectomy: incidence and time. J. Surg. Res. 163, 69–71 (2010)

    CAS  PubMed  Google Scholar 

  11. M.I. Khan, S.G. Waguespack, M.I. Hu, Medical management of postsurgical hypoparathyroidism. Endocr. Pract. 17, 18–25 (2011)

    PubMed  Google Scholar 

  12. D. Giordano, R. Valcavi, G.B. Thompson, C. Pedroni, L. Renna, P. Gradoni, V. Barbieri, Complications of central neck dissection in patients with papillary thyroid carcinoma: results of a study on 1087 patients and review of the literature. Thyroid 22, 911–917 (2012)

    PubMed  Google Scholar 

  13. S.H. Paek, Y.M. Lee, S.Y. Min, S.W. Kim, K.W. Chung, Y.K. Youn, Risk factors of hypoparathyroidism following total thyroidectomy for thyroid cancer. World J. Surg. 37, 94–101 (2013).

    PubMed  Google Scholar 

  14. A. Puzziello, L. Rosato, N. Innaro, G. Orlando, N. Avenia, G. Perigli, P.G. Calò, M. De Palma, Hypocalcemia following thyroid surgery: incidence and risk factors. A longitudinal multicenter study comprising 2,631 patients. Endocrine 47, 537–542 (2014)

    CAS  PubMed  Google Scholar 

  15. O. Edafe, R. Antakia, N. Laskar, L. Uttley, S.P. Balasubramanian, Systematic review and meta-analysis of predictors of post-thyroidectomy hipocalcemia. Br. J. Surg. 101, 307–320 (2014)

    CAS  PubMed  Google Scholar 

  16. K. Ritter, D. Elfenbein, D.F. Schneider, D.F. Schneider, H. Chen, R.S. Sippel, Hypoparathyroidism after total thyroidectomy: incidence and resolution. J. Surg. Res. 197, 348–353 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  17. X. Wang, T. Xing, T. Wei, J. Zhu, Completion thyroidectomy and total thyroidectomy for differentiated thyroid cancer: comparison and prediction of postoperative hypoparathyroidism. J. Surg. Oncol. 113, 522–525 (2016)

    PubMed  Google Scholar 

  18. S.A. Hundahl, B. Cady, M.P. Cunningham, I. Mazzaferri, R.F. McKee, J. Rosai, J.P. Shah, A.M. Fremgen, A.K. Stewart, S. Hölzer, 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 (2000)

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  20. A. Bergenfelz, S. Jansson, A. Kristofferson, H. Martenson, E. Reihnér, G. Wallin, I. Lausen, Complications to thyroid surgery: results as reported in a database from a multicenter audit comprising 3660 patients. Lange. Arch. Surg. 393, 667–673 (2008)

    CAS  Google Scholar 

  21. J.J. Jeong, S.W. Kang, J.S. Yun, T.Y. Sung, S.C. Lee, Y.S. Lee, K.H. Nam, H.S. Chang, W.Y. Chung, C.S. Park, Comparative study of endoscopic thyroidectomy versus conventional open thyroidectomy in papillary thyroid microcarcinoma (PTMC) patients. J. Surg. Oncol. 100, 477–480 (2009)

    PubMed  Google Scholar 

  22. D. Shoback, Clinical practice. Hypoparathyroidism. N. Engl. J. Med. 359, 391–403 (2008)

    CAS  PubMed  Google Scholar 

  23. L.A. Orloff, S.M. Wiseman, V.J. Bernet, T.J. Faheylll, A.R. Shaha, M.L. Shindo, S.K. Snyder, B.C. Stack Jr, J.B. Sunwoo, M.B. Wang, American Thyroid Association statement on postoperative hypoparathyroidism: diagnosis, prevention, and management in adults. Thyroid 28, 830–841 (2018)

    PubMed  Google Scholar 

  24. S.M. Kim, H.K. Kim, K.J. Kim, H.J. Chang, B.W. Kim, Y.S. Lee, H.S. Chang, C.S. Park, Recovery from permanent hypoparathyroidism after total thyroidectomy. Thyroid 25, 830–833 (2015)

    CAS  PubMed  Google Scholar 

  25. I. Villarroya-Marquina, J. Sancho, L. Lorente-Poch, L. Gallego-Otaegui, A. Sitges-Serra, Time to parathyroid function recovery in patients with protracted hypoparathyroidism after total thyroidectomy. Eur. J. Endocrinol. 178, 103–111 (2018)

    CAS  PubMed  Google Scholar 

  26. J. Powers, K. Joy, A. Ruscio, H. Lagast, Prevalence and incidence of hypoparathyroidism in the United States using a large claims database. J. Bone Miner. Res. 28, 2570–2576 (2013)

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  28. L. Lorente-Poch, J.J. Sancho, J.L. Muñoz-Nova, P. Sánchez-Velázquez, A. Sitges-Serra, Defining the syndromes of parathyroid failure after total thyroidectomy. Gland Surg. 4, 82–90 (2015)

    PubMed  PubMed Central  Google Scholar 

  29. O. Thomusch, A. Machens, C. Sekulla, J. Ukkat, M. Brauckhoff, H. Dralle, The impact of surgical technique on postoperative hypoparathyroidism in bilateral thyroid surgery: a multivariate analysis of 5846 consecutive patients. Surgery 133, 180–185 (2003)

    PubMed  Google Scholar 

  30. Y. Erbil, A. Bozbora, N. Ozbey, H. Issever, F. Aral, S. Ozarmagan, S. Tezelman, Predictive value of age and serum parathormone and vitamin D3 levels for postoperative hypocalcemia after total thyroidectomy for nontoxic multinodular goiter. Arch. Surg. 142, 1182–1187 (2007)

    CAS  PubMed  Google Scholar 

  31. P. Hallgrimsson, E. Nordenström, M. Almquist, A.O. Bergenfelz, Risk factors for medically treated hypocalcemia after surgery for Graves’ disease: a Swedish multicenter study of 1157 patients. World J. Surg. 36, 1933–1942 (2012)

    CAS  PubMed  Google Scholar 

  32. L. Lorente-Poch, J.J. Sancho, S. Ruiz, A. Sitges-Serra, Importance of in situ preservation of parathyroid glands during total thyroidectomy. Br. J. Surg. 102, 359–367 (2015)

    CAS  PubMed  Google Scholar 

  33. B.H. Lang, P.C. Yih, K.K. Ng, A prospective evaluation of quick intraoperative parathyroid hormone assay at the time of skin closure in predicting clinically relevant hypocalcemia after thyroidectomy. World J. Surg. 36, 1300–1306 (2012)

    PubMed  PubMed Central  Google Scholar 

  34. C.Y. Lo, Parathyroid autotransplantation during thyroidectomy. ANZ J. Surg. 72, 902–907 (2002)

    PubMed  Google Scholar 

  35. J.A. Pereira, J. Jimeno, J. Miquel, M. Iglesias, A. Munné, J.J. Sancho, A. Sitges-Serra, Nodal yield, morbidity, and recurrence after central neck dissection for papillary thyroid carcinoma. Surgery 138, 1095–1100 (2005).

    PubMed  Google Scholar 

  36. J.A. Olson Jr, M.K. DeBenedetti, D.S. Baumann, S.A. Wells Jr, Parathyroid autotransplantation during thyroidectomy. Results of long-term follow-up. Ann. Surg. 223, 472–478 (1996).

    PubMed  PubMed Central  Google Scholar 

  37. C.Y. Lo, S.C. Tam, Parathyroid autotransplantation during thyroidectomy: documentation of graft function. Arch. Surg. 136, 1381–1385 (2001)

    CAS  PubMed  Google Scholar 

  38. M. Almquist, P. Hallgrimsson, E. Nordenström, A. Bergenfelz, Prediction of permanent hypoparathyroidism after total thyroidectomy. World J. Surg. 38, 2613–2620 (2014)

    CAS  PubMed  Google Scholar 

  39. F. Pattou, F. Combemale, S. Fabre, B. Carnaille, M. Decoulx, J.L. Wemeau, A. Racadot, C. Prove, Hypocalcemia following thyroid surgery: incidence and prediction of outcome. World J. Surg. 22, 718–724 (1998)

    CAS  PubMed  Google Scholar 

  40. U. Ohman, P.O. Granberg, B. Lindell, Function of the parathyroid glands after total thyroidectomy. Surg. Gynecol. Obstet. 146, 773–778 (1978)

    CAS  PubMed  Google Scholar 

  41. R. Bergamaschi, G. Becouarn, J. Ronceray, J.P. Arnaud, Morbidity of thyroid surgery. Am. J. Surg. 176, 71–75 (1998)

    CAS  PubMed  Google Scholar 

  42. O. Thomusch, A. Machens, C. Sekulla, J. Ukkat, H. Lippert, I. Gastinger, H. Dralle, Multivariate analysis of risk factors for postoperative complications in benign goiter surgery: prospective multicenter study in Germany. World J. Surg. 24, 1335–1341 (2000)

    CAS  PubMed  Google Scholar 

  43. W.K. Cheah, C. Arici, P.H. Ituarte, A.E. Siperstein, Q.Y. Duh, O.H. Clark, Complications of neck dissection for thyroid cancer. World J. Surg. 26, 1013–1016 (2002)

    PubMed  Google Scholar 

  44. J.F. Henry, L. Gramatica, A. Denizot, A. Kvachenyuk, M. Puccini, T. Defechereux, Morbidity of prophylactic lymph node dissection in the central neck area in patients with papillary thyroid carcinoma. Lange. Arch. Surg. 383, 167–169 (1998)

    CAS  Google Scholar 

  45. M. Hermann, J. Ott, R. Promberger, F. Kober, M. Karik, M. Freissmuth, Kinetics of serum parathyroid hormone during and after thyroid surgery. Br. J. Surg. 95, 1480–1487 (2008)

    CAS  PubMed  Google Scholar 

  46. A. Sitges-Serra, J. Gómez, M. Barczynski, L. Lorente-Poch, M. Iacobone, J. Sancho, A nomogram to predict the likelihood of permanent hypoparathyroidism after total thyroidectomy based on delayed serum calcium and iPTH measurements. Gland Surg. 6(Suppl 1), S11–S19 (2017)

    PubMed  PubMed Central  Google Scholar 

  47. O. Cavicchi, O. Piccin, U. Caliceti, A. De Cataldis, R. Pasquali, A.R. Ceroni, Transient hypoparathyroidism following thyroidectomy: a prospective study and multivariate analysis of 604 consecutive patients. Otolaryngol. Head. Neck Surg. 137, 654–658 (2007)

    PubMed  Google Scholar 

  48. I. Nawrot, A. Pragacz, K. Pragacz, W. Grzesiuk, M. Barczynski, Total thyroidectomy is associated with increased prevalence of permanent hypoparathyroidism. Med. Sci. Monit. 20, 1675–1681 (2014)

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Author notes

  1. Juan J. Díez & Pedro Iglesias

    Present address: Department of Endocrinology, Hospital Universitario Puerta de Hierro Majadahonda, Madrid, Spain

Authors and Affiliations

  1. Department of Endocrinology, Hospital Universitario Ramón y Cajal, Madrid, Spain

    Juan J. Díez & Pedro Iglesias

  2. Department of Endocrinology, Complejo Hospitalario de Navarra, Pamplona, Spain

    Emma Anda

  3. Department of Endocrinology, Complejo Hospitalario de Toledo, Toledo, Spain

    Julia Sastre

  4. Department of Endocrinology, Complejo Asistencial Universitario de León, León, Spain

    Begoña Pérez Corral

  5. Department of Endocrinology, Hospital Universitario La Paz, Madrid, Spain

    Cristina Álvarez-Escolá & Beatriz Lecumberri

  6. Department of Endocrinology, Hospital Universitario Central de Asturias, Oviedo, Spain

    Laura Manjón & Cecilia Sánchez Ragnarsson

  7. Department of Endocrinology, Hospital Universitario de Basurto, Bilbao, Spain

    Miguel Paja & Amelia Oleaga

  8. Department of Endocrinology, Hospital Universitario Gregorio Marañón, Madrid, Spain

    Marcel Sambo & María Picallo

  9. Department of Endocrinology, Complejo Hospitalario de Jaén, Jaén, Spain

    Piedad Santiago Fernández

  10. Department of Endocrinology, Hospital Universitario Príncipe de Asturias, Alcalá de Henares, Madrid, Spain

    Concepción Blanco Carrera

  11. Department of Endocrinology, Clínica Universidad de Navarra, Pamplona, Spain

    Juan C Galofré

  12. Department of Endocrinology, Hospital Universitario Virgen del Rocío, Sevilla, Spain

    Elena Navarro & Ana R. Romero-Lluch

  13. Department of Endocrinology, Hospital Universitari Vall d’Hebron, Barcelona, Spain

    Carles Zafón & Eva Sanz

  14. Department of Endocrinology, Hospital Royo Villanova, Zaragoza, Spain

    Orosia Bandrés

  15. Department of Endocrinology, Fundación Hospital de Alcorcón, Alcorcón, Madrid, Spain

    Sergio Donnay

  16. Department of Endocrinology, Hospital Universitario de Tarragona Joan XXIII, IISPV, Universitat Rovira i Virgili, Ciberdem, Tarragona, Spain

    Ana Megía

  17. Department of Endocrinology, Hospital de Jerez, Jerez de la Frontera, Cádiz, Spain

    Gloria Baena-Nieto

  18. Department of Endocrinology, Hospital Virgen de la Victoria, Málaga, Spain

    José Carlos Fernández García

  19. Department of Endocrinology, Hospital Moisès Broggi, Sant Joan Despí, Barcelona, Spain

    Manel Sahún de la Vega

Authors
  1. Juan J. Díez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emma Anda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julia Sastre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Begoña Pérez Corral
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cristina Álvarez-Escolá
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Laura Manjón
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Miguel Paja
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marcel Sambo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Piedad Santiago Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Concepción Blanco Carrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Juan C Galofré
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Elena Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Carles Zafón
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Eva Sanz
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Amelia Oleaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Orosia Bandrés
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Sergio Donnay
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Ana Megía
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. María Picallo
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Cecilia Sánchez Ragnarsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Gloria Baena-Nieto
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. José Carlos Fernández García
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Beatriz Lecumberri
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Manel Sahún de la Vega
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Ana R. Romero-Lluch
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Pedro Iglesias
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan J. Díez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original version of this article was revised: the given and family name of Juan Carlos Galofré was corrected.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Díez, J.J., Anda, E., Sastre, J. et al. Prevalence and risk factors for hypoparathyroidism following total thyroidectomy in Spain: a multicentric and nation-wide retrospective analysis. Endocrine 66, 405–415 (2019). https://doi.org/10.1007/s12020-019-02014-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-019-02014-8

Keywords

Search

Navigation