Abstract
Purpose
To describe the outcomes and the incidence of adverse events following active surveillance (AS) versus immediate surgery in patients with low-risk papillary thyroid carcinoma (PTC).
Methods
We prospectively evaluated 286 patients who attended the Hospital de Clínicas, with a single thyroid nodule <1.5 cm classified as Bethesda category V or VI (PTC). Those patients with no aggressive features were considered as harboring a low-risk PTC and were offered AS or immediate surgery. For patients who opted for AS, surgery was recommended if tumor progression was observed. Post-operative adverse events were recorded for those patients treated with surgery (after AS or immediate surgery).
Results
From 286 eligible patients, 164 harbored a low-risk PTC. Among these, 75% (n = 123) underwent immediate surgery and 25% (n = 41) opted for AS. Within the last group, increase in tumor size more than 3 mm was observed in 14.6 and 4.8% was diagnosed with lymph-node metastases after a median of 37.5 months (range, 12–65) of follow-up. One hundred and thirty five patients underwent surgery: in 123, it was immediate after diagnosis and in 12 after a median of 35 months (range, 12–65) of AS. Both groups had excellent oncological outcomes. The frequency of postoperative adverse events was 24.4%, which was permanent in 9.6% of cases. The immediate-surgery group presented higher incidence of permanent vocal cord paralysis (2.4 vs. 0%); permanent hypoparathyroidism (5.7 vs. 0%) and local complications (4 vs. 2.4%) compared with the AS group, all non-statistically significant.
Conclusions
The high incidence of postoperative complications observed in our media could be avoided if AS was performed as the initial approach in patients with low-risk PTCs. The frequency of tumor growth and LN metastases during AS was similar to other series.
Similar content being viewed by others
References
L. Davies, L.G. Morris, M. Haymart, A.Y. Chen, D. Goldenberg, J. Morris, J.B. Ogilvie, D.J. Terris, J. Netterville, R.J. Wong, G. Randolph, AACE Endocrine Surgery Scientific Committee: American association of clinical endocrinologists and american college of endocrinology disease state clinical review: the increasing incidence of thyroid cancer. Endocr. Pract. 21, 686–696 (2015)
L. Davies, H.G. Welch, Current thyroid cancer trends in the United States. JAMA Otolaryngol. Head. Neck Surg. 140, 317–322 (2014)
Y. Ito, T. Uruno, K. Nakano, Y. Takamura, A. Miya, K. Kobayashi, T. Yokozawa, F. Matsuzuka, S. Kuma, K. Kuma, A. Miyauchi, An observation trial without surgical treatment in patients with papillary microcarcinoma of the thyroid. Thyroid 13, 381–387 (2013)
H.R. Harach, K.O. Franssila, V.M. Wasenius, Occult papillary carcinoma of the thyroid. A “normal” finding in finland. A systematic autopsy study. Cancer 56, 531–538 (1985)
Y. Ito, A. Miyauchi, H. Inoue, M. Fukushima, M. Kihara, T. Higashiyama, C. Tomoda, Y. Takamura, K. Kobayashi, A. Miya, An observational trial for papillary thyroid microcarcinoma in Japanese patients. World J. Surg. 34(1), 28–35 (2016)
H. Oda, A. Miyauchi, Y. Ito, K. Yoshioka, A. Nakayama, H. Sasai, H. Masuoka, T. Yabuta, M. Fukushima, T. Higashiyama, M. Kihara, K. Kobayashi, A. Miya, Incidences of unfavorable events in the management of low-risk papillary microcarcinoma of the thyroid by active surveillance versus immediate surgery. Thyroid 26, 150–155 (2016)
B.R. Haugen, E.K. Alexander, K.C. Bible, G.M. Doherty, S.J. Mandel, Y.E. Nikiforov, F. Pacini, G.W. Randolph, A.M. Sawka, M. Schlumberger, K.G. Schuff, S.I. Sherman, J.A. Sosa, D.L. Steward, R.M. Tuttle, L. Wartofsky, 2015 American thyroid association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American thyroid association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid 26, 1–133 (2016)
F. Pitoia, I. Califano, A. Vázquez, E. Faure, A. Gauna, A. Orlandi, A. Vanelli, J.L. Novelli, A. Mollerach, A. Fadel, A. San Martín, M. Figari, C. Cabezón, Inter society consensus for the management of patients with differentiated thyroid cancer. Rev. Argent. de. Endocrinol.ía y. Metab. 51, 85–118 (2014)
L. Rosato, N. Avenia, P. Bernante, M. De Palma, G. Gulino, P.G. Nasi, M.R. Pelizzo, L. Pezzullo, Complications of thyroid surgery: analysis of a multicentric study on 14,934 patients operated on in italy over 5 years. World J. Surg. 28, 271–276 (2004)
J.A. Sosa, H.M. Bowman, J.M. Tielsch, N.R. Powe, T.A. Gordon, R. Udelsman, The importance of surgeon experience for clinical and economic outcomes from thyroidectomy. Ann. Surg. 228, 320–330 (1998)
A. Hauch, Z. Al-Qurayshi, G. Randolph, E. Kandil, Total thyroidectomy is associated with increased risk of complications for low- and high- volume. Ann. Surgical Oncol. 21(12), 3844–3852 (2014)
Y. Ito, A. Miyauchi, A therapeutic strategy for incidentally detected papillary microcarcinoma of the thyroid. Nat. Clin. Pr. Endocrin Metab. 3(3), 240–248 (2007)
R.M. Tuttle, J.A. Fagin, G. Minkowitz, R.J. Wong, B. Roman, S. Patel, B. Untch, I. Ganly, A.R. Shaha, J.P. Shah, M. Pace, D. Li, A. Bach, O. Lin, A. Whiting, R. Ghossein, I. Landa, M. Sabra, L. Boucai, S. Fish, L.G.T. Morris, Natural history and tumor volume kinetics of papillary thyroid cancers during active surveillance. JAMA Otolaryngol. Head. Neck Surg. 143(10), 1015–1020 (2017)
Y. Ito, A. Miyauchi, H. Oda, Low-risk papillary microcarcinoma of the thyroid: a review of active surveillance trials. Eur. J. Surg. Oncol. 44(3), 307–315 (2018)
Y. Ito, A. Miyauchi, M. Kihara, T. Higashiyama, K. Kobayashi, A. Miya, Patient age is significantly related to the progression of papillary microcarcinoma of the thyroid under observation. Thy 181, 72–79 (2014)
A. Smulever, F. Pitoia, Active surveillance in papillary thyroid carcinoma: not easily accepted but possible in Latin America. Arch. Endocrinol. Metab. 63(5), 462–469 (2019)
J.P. Brito, Y. Ito, A. Miyauchi, R.M. Tuttle, A clinical framework to facilitate risk stratification when considering an active surveillance alternative to immediate biopsy and surgery in papillary microcarcinoma. Thy 26, 144–149 (2015)
R.M. Tuttle, L. Zhang, A. Shaha, A clinical framework to facilitate selection of patients with differentiated thyroid cancer for active surveillance or less aggressive initial surgical management. Expert Rev. Endocrinol. Metab. 13, 77–85 (2018)
L. Orloff, S. Wiseman, V. Bernet, T. Fahey, A. Shaha, M. Shindo, S. Snyder, B. Stack, J. Sunwoo, M. Wang, American thyroid association statement on postoperative hypoparathyroidism: diagnosis, prevention, and management in adults. Thyroid 28(7), 830–841 (2018)
R.S. Prichard, P.J. Edhouse, S.B. Sidhu, M.S. Sywak, L. Delbridge, Post-operative partial hypoparathyroidism: an under-recognized disorder. ANZ J. Surg. 82(1-2), 93–94 (2012)
D.P. Momesso, F. Vaisman, S.P. Yang, D.A. Bulzico, R. Corbo, M. Vaisman et al. Dynamic risk stratification in patients with differentiated thyroid cancer treated without radioactive iodine. J. Clin. Endocrinol. Metab. 101(7), 2692–2700 (2016)
K. Mitsuzuka, H. Koga, M. Sugimoto, Y. Arai, C. Ohyama, Y. Kakehi, S. Naito, Current use of active surveillance for localized prostate cancer: a nationwide survey in Japan. Int J. Urol. 22(8), 754–759 (2015)
H. Kwon, H.S. Oh, M. Kim, S. Park, M.J. Jeon, W.G. Kim, W.B. Kim, Y.K. Shong, D.E. Song, J.H. Baek, K.W. Chung, T.Y. Kim, Active surveillance for patients with papillary thyroid microcarcinoma: a single center’s experience in Korea. The. J. Clin. Endocrinol. Metab. 102, 1917–1925 (2017)
H. Takami, Y. Ito, T. Okamoto, N. Onoda, H. Noguchi, A. Yoshida, Revisiting the guidelines issued by the Japanese Society of Thyroid Surgeons and Japan Association of Endocrine Surgeons: a gradual move towards consensus between Japanese and western practice in the management of thyroid carcinoma. World J. Surg. 38, 2002–2010 (2014)
E. Molinaro, M.C. Campopiano, L. Pieruzzi, A. Matrone, L. Agate, V. Bottici, D. Viola, V. Cappagli, L. Valerio, C. Giani, L. Puleo, L. Lorusso, P. Piaggi, L. Torregrossa, F. Basolo, P. Vitti, R.M. Tuttle, R. Elisei, Active surveillance in papillary thyroid microcarcinomas is feasible and safe:experience at one single Italian center. J. Clin. Endocrinol. Metab. 150(3), dgz113 (2019)
T. Sakai, I. Sugitani, A. Ebina, O. Fukuoka, K. Toda, H. Mitani, K. Yamada, Active surveillance for T1bN0M0 papillary thyroid carcinoma. Thyroid 29, 59–63 (2018)
A. Miyauchi, T. Kudo, Y. Ito, H. Oda, M. Yamamoto, H. Sasai, T. Higashiyama, H. Masuoka, M. Fukushima, M. Kihara, A. Miya, Natural history of papillary thyroid microcarcinoma: kinetic analyses on tumor volume during active surveillance and before presentation. Surgery 165(1), 25–30 (2018)
D.M. Hartl, M. Schlumberger, Extent of thyroidectomy and incidence of morbidity. Thyroid Surg. 20, 19–32 (2013)
J.F. Lin, P.K.C. Jonker, M. Cunich, S.B. Sidhu, L.W. Delbridge, A.R. Glover, D.L. Learoyd, A. Aniss, S. Kruijff, M.S. Sywak, Surgery alone for papillary thyroid microcarcinoma is less costly and more effective than long term active surveillance. Surgery 167(1), 110–116 (2020)
H. Verloop, M. Louwerens, J.W. Schoones, J. Kievit, J.W. Smit, O.M. Dekkers, Risk of hypothyroidism following hemithyroidectomy: systematic review and meta-analysis of prognostic studies. J. Clin. Endocrinol. Metab. 97, 2243–2255 (2012)
L. Lamartina, C. Durante, G. Lucisano, G. Grani, R. Bellantone, C.P. Lombardi, A. Pontecorvi, E. Arvat, F. Felicetti, M.C. Zatelli, R. Rossi, E. Puxeddu, S. Morelli, M. Torlontano, U. Crocetti, T. Montesano, R. Giubbini, F. Orlandi, G. Aimaretti, F. Monzani, M. Attard, C. Francese, A. Antonelli, P. Limone, R. Rossetto, L. Fugazzola, D. Meringolo, R. Bruno, S. Tumino, G. Ceresini, M. Centanni, S. Monti, D. Salvatore, G. Spiazzi, C. Mian, L. Persani, D. Barbaro, A. Nicolucci, S. Filetti, Are evidence-based guidelines reflected in clinical practice? An analysis of prospectively collected data of the italian thyroid cancer observatory. Thyroid 27(12), 1490–1497 (2017)
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by AS and FP. The first draft of the paper was written by AS and FP and all authors commented on previous versions of the paper. All authors read and approved the final paper.
Corresponding author
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.
Rights and permissions
About this article
Cite this article
Smulever, A., Pitoia, F. High rate incidence of post-surgical adverse events in patients with low-risk papillary thyroid cancer who did not accept active surveillance. Endocrine 69, 587–595 (2020). https://doi.org/10.1007/s12020-020-02310-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12020-020-02310-8