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Long-term follow-up ultrasonography surveillance in a large cohort of patients with papillary thyroid carcinoma

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Abstract

Objective

This study aimed to investigate the predictive factors as well as the time and age course of recurrence/persistence in a large cohort of postoperative patients with papillary thyroid carcinoma (PTC) based on the long-term ultrasonography (US) follow-up data.

Methods

Between January 2007 and December 2016, 3106 patients underwent surgery for PTC and at least two postoperative US follow-up examination over more than three years. Tumor recurrence/persistence was confirmed based on the follow-up US data and histopathological results. Univariate and multivariate analyses were performed to evaluate the predictive factors of tumor recurrence/persistence. Kaplan–Meier survival analysis was used to evaluate the recurrence-/persistence-free survival curve based on the US results.

Results

A total of 321(10.3%) patients developed tumor recurrence/persistence during 54.3 months of mean follow-up (range 36–135 months), including 268(83.5%) cases of lymph node recurrence/persistence, 37 (11.5%) cases of non-lymph node recurrence/persistence, and 16(5%) cases of both types. Recurrence/persistence was observed using US examination at a mean interval of 23.6 ± 21.6 months (range 1–135 months) after surgery and peak incidence was observed 1–2 years after initial treatment. Younger (20–30 years old) and older (70–80 years old) patients had a higher proportion of tumor recurrence/persistence. Multifocality, advanced T and advanced N stages were independent risk factors of tumor recurrence/persistence.

Conclusion

Tumor recurrence/persistence of PTC usually occurs during the early postoperative period. For patients with multifocal cancer, advanced T and N stage, the US surveillance examination should be cautiously performed, especially in younger and older patients.

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References

  1. R.M. Tuttle, B. Haugen, N.D. Perrier. Updated American Joint Committee on cancer/tumor-node-metastasis staging system for differentiated and anaplastic thyroid cancer: what changed and why? (Mary Ann Liebert, Inc., 140 Huguenot Street, 3rd Floor New Rochelle, NY 10801 USA, 2017)

  2. A. Pisanu, I. Reccia, O. Nardello, A. Uccheddu, Risk factors for nodal metastasis and recurrence among patients with papillary thyroid microcarcinoma: differences in clinical relevance between nonincidental and incidental tumors. World journal of surgery 33, 460 (2009)

    Article  Google Scholar 

  3. C.S. Grant, I.D. Hay, I.R. Gough, E.J. Bergstralh, J.R. Goellner, W.M. McConahey, Local recurrence in papillary thyroid carcinoma: is extent of surgical resection important? Surgery 104, 954–962 (1988)

    CAS  PubMed  Google Scholar 

  4. H.K. Park, D.W. Kim, T.K. Ha, Y.J. Heo, J.W. Baek, Y.J. Lee, Y.J. Cho, D.K. Lee, D.H. Kim, S.J. Jung, Utility of routine ultrasonography follow-up after total thyroidectomy in patients with papillary thyroid carcinoma: a single-center study. BMC medical imaging 18, 12 (2018)

    Article  Google Scholar 

  5. E.L. Mazzaferri, S.M. Jhiang, Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. The American journal of medicine 97, 418–428 (1994)

    Article  CAS  Google Scholar 

  6. Y.J. Lee, D.W. Kim, G.W. Shin, Y.J. Heo, J.W. Baek, Y.J. Cho, Y.M. Park, H.K. Park, T.K. Ha, D.H. Kim, Appropriate Frequency and interval of neck Ultrasonography surveillance during the First 10 Years after Total Thyroidectomy in Patients with Papillary Thyroid carcinoma. Frontiers in endocrinology 9, 79 (2018)

    Article  Google Scholar 

  7. C.S. Grant, Recurrence of papillary thyroid cancer after optimized surgery. Gland surgery 4, 52 (2015)

    PubMed  PubMed Central  Google Scholar 

  8. I. Ryoo, D.W. Kim, C.Y. Lee, J.Y. Huh, S. Lee, H.S. Ahn, J.Y. Sung, Analysis of postoperative ultrasonography surveillance after total thyroidectomy in patients with papillary thyroid carcinoma: a multicenter study. Acta Radiologica 59, 196–203 (2018)

    Article  Google Scholar 

  9. M. Torlontano, M. Attard, U. Crocetti, S. Tumino, R. Bruno, G. Costante, G. D’Azzò, D. Meringolo, E. Ferretti, R. Sacco, Follow-up of low risk patients with papillary thyroid cancer: role of neck ultrasonography in detecting lymph node metastases. The Journal of Clinical Endocrinology & Metabolism 89, 3402–3407 (2004)

    Article  CAS  Google Scholar 

  10. M.C. Frates, C.B. Benson, J.W. Charboneau, E.S. Cibas, O.H. Clark, B.G. Coleman, J.J. Cronan, P.M. Doubilet, D.B. Evans, J.R. Goellner, Management of thyroid nodules detected at US: Society of Radiologists in Ultrasound consensus conference statement. Radiology 237, 794–800 (2005)

    Article  Google Scholar 

  11. H. Pelttari, K. Laitinen, C. Schalin-Jäntti, M.J. Välimäki, Long-term outcome of 495 TNM stage I or II patients with differentiated thyroid carcinoma followed up with neck ultrasonography and thyroglobulin measurements on T4 treatment. Clinical endocrinology 69, 323–331 (2008)

    Article  CAS  Google Scholar 

  12. M.A. Kouvaraki, S.E. Shapiro, B.D. Fornage, B.S. Edeiken-Monro, S.I. Sherman, R. Vassilopoulou-Sellin, J.E. Lee, D.B. Evans, Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 134, 946–954 (2003)

    Article  Google Scholar 

  13. A. Frasoldati, M. Pesenti, M. Gallo, A. Caroggio, D. Salvo, R. Valcavi, Diagnosis of neck recurrences in patients with differentiated thyroid carcinoma. Cancer 97, 90–96 (2003)

    Article  Google Scholar 

  14. F. Pacini, E. Molinaro, M. Castagna, L. Agate, R. Elisei, C. Ceccarelli, F. Lippi, D. Taddei, L. Grasso, A. Pinchera, Recombinant human thyrotropin-stimulated serum thyroglobulin combined with neck ultrasonography has the highest sensitivity in monitoring differentiated thyroid carcinoma. The Journal of Clinical Endocrinology & Metabolism 88, 3668–3673 (2003)

    Article  CAS  Google Scholar 

  15. M. Torlontano, U. Crocetti, L. D’Aloiso, N. Bonfitto, A. Di Giorgio, S. Modoni, G. Valle, V. Frusciante, M. Bisceglia, S. Filetti, Serum thyroglobulin and 131I whole body scan after recombinant human TSH stimulation in the follow-up of low-risk patients with differentiated thyroid cancer. European Journal of Endocrinology 148, 19–24 (2003)

    Article  CAS  Google Scholar 

  16. L. Davies, H. Welch, Current thyroid cancer trends in the United States. JAMA Otolaryngol Head Neck Surg 140(4), 317–322 (2014)

    Article  Google Scholar 

  17. S.F. Hall, H. Walker, R. Siemens, A. Schneeberg, Increasing detection and increasing incidence in thyroid cancer. World J Surg 33, 2567–2571 (2009)

    Article  Google Scholar 

  18. 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, 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: official journal of the American Thyroid Association 26, 1–133 (2016)

    Article  Google Scholar 

  19. L. Leenhardt, M. Erdogan, L. Hegedus, S. Mandel, R. Paschke, T. Rago, G. Russ, 2013 European thyroid association guidelines for cervical ultrasound scan and ultrasound-guided techniques in the postoperative management of patients with thyroid cancer. European thyroid journal 2, 147–159 (2013)

    Article  CAS  Google Scholar 

  20. S. Zaheer, A. Tan, E.S. Ang, K.S. Loke, Y.H. Kao, A. Goh, W.Y. Wong, Post-thyroidectomy neck ultrasonography in patients with thyroid cancer and a review of the literature. Singapore medical journal 55, 177 (2014)

    Article  Google Scholar 

  21. D. Minami, N. Takigawa, H. Hayakawa, M. Mizuta, K. Kudo, K. Uchida, E. Ichihara, A. Sato, K. Hotta, M. Tabata, Usefulness of endobronchial ultrasound-guided transbronchial needle aspiration in distinguishing sarcoidosis from recurrent cancer in patients with lymphadenopathy after surgery. Japanese journal of clinical oncology 43, 1110–1114 (2013)

    Article  Google Scholar 

  22. Y. Ito, T. Kudo, K. Kobayashi, A. Miya, K. Ichihara, A. Miyauchi, Prognostic factors for recurrence of papillary thyroid carcinoma in the lymph nodes, lung, and bone: analysis of 5,768 patients with average 10-year follow-up. World journal of surgery 36, 1274–1278 (2012)

    Article  Google Scholar 

  23. H.J. Kim, S.Y. Sohn, H.W. Jang, S.W. Kim, J.H. Chung, Multifocality, but not bilaterality, is a predictor of disease recurrence/persistence of papillary thyroid carcinoma. World journal of surgery 37, 376–384 (2013)

    Article  Google Scholar 

  24. G. Sapuppo, F. Palermo, M. Russo, M. Tavarelli, R. Masucci, S. Squatrito, R. Vigneri, G. Pellegriti, Latero-cervical lymph node metastases (N1b) represent an additional risk factor for papillary thyroid cancer outcome. Journal of endocrinological investigation 40, 1355–1363 (2017)

    Article  CAS  Google Scholar 

  25. C.W. Lee, J.L. Roh, G. Gong, K.J. Cho, S.H. Choi, S.Y. Nam, S.Y. Kim, Risk factors for recurrence of papillary thyroid carcinoma with clinically node-positive lateral neck. Ann Surg Oncol 22, 117–124 (2015)

    Article  Google Scholar 

  26. S.H. Lee, J.L. Roh, G. Gong, K.J. Cho, S.H. Choi, S.Y. Nam, S.Y. Kim, Risk factors for recurrence after treatment of N1b papillary thyroid carcinoma. Annals of surgery 269, 966–971 (2019)

    Article  Google Scholar 

  27. G. Sapuppo, M. Tavarelli, A. Belfiore, R. Vigneri, G. Pellegriti, Time to separate persistent from recurrent differentiated thyroid cancer: different conditions with different outcomes. J Clin Endocrinol Metab 104, 258–265 (2019)

    Article  Google Scholar 

  28. A. Al Afif, B.A. Williams, M.H. Rigby, M.J. Bullock, S.M. Taylor, J. Trites, R.D. Hart, Multifocal papillary thyroid cancer increases the risk of central lymph node metastasis. Thyroid: official journal of the American Thyroid Association 25, 1008–1012 (2015)

    Article  Google Scholar 

  29. W. Wang, W. Zhao, H. Wang, X. Teng, H. Wang, X. Chen, Z. Li, X. Yu, T.J. Fahey, L. Teng, Poorer prognosis and higher prevalence of BRAF V600E mutation in synchronous bilateral papillary thyroid carcinoma. Annals of surgical oncology 19, 31–36 (2012)

    Article  Google Scholar 

  30. S. Leboulleux, C. Rubino, E. Baudin, B. Caillou, D.M. Hartl, J.-M. Bidart, J.-P. Travagli, M. Schlumberger, Prognostic factors for persistent or recurrent disease of papillary thyroid carcinoma with neck lymph node metastases and/or tumor extension beyond the thyroid capsule at initial diagnosis. The Journal of clinical endocrinology and metabolism 90, 5723–5729 (2005)

    Article  CAS  Google Scholar 

  31. A.M. Schindler, G. van Melle, B. Evequoz, B. Scazziga, Prognostic factors in papillary carcinoma of the thyroid. Cancer 68, 324–330 (1991)

    Article  CAS  Google Scholar 

  32. L. Yang, W. Shen, N. Sakamoto, Population-based study evaluating and predicting the probability of death resulting from thyroid cancer and other causes among patients with thyroid cancer. Journal of clinical oncology 31, 468–474 (2013)

    Article  Google Scholar 

  33. G.W. Randolph, Q.-Y. Duh, K.S. Heller, V.A. LiVolsi, S.J. Mandel, D.L. Steward, R.P. Tufano, R. Michael Tuttle; ftATASACsToTCNS, The prognostic significance of nodal metastases from papillary thyroid carcinoma can be stratified based on the size and number of metastatic lymph nodes, as well as the presence of extranodal extension. Thyroid: official journal of the American Thyroid Association 22, 1144–1152 (2012)

    Article  Google Scholar 

  34. S.-K. Baek, K.-Y. Jung, S.-M. Kang, S.-Y. Kwon, J.-S. Woo, S.-H. Cho, E.-J. Chung, Clinical risk factors associated with cervical lymph node recurrence in papillary thyroid carcinoma. Thyroid: official journal of the American Thyroid Association 20, 147–152 (2010)

    Article  Google Scholar 

  35. Y.C. Lee, S.Y. Na, G.C. Park, J.H. Han, S.W. Kim, Y.G. Eun, Occult lymph node metastasis and risk of regional recurrence in papillary thyroid cancer after bilateral prophylactic central neck dissection: a multi-institutional study. Surgery 161, 465–471 (2017)

    Article  Google Scholar 

  36. S.Y. Kim, J.Y. Kwak, E.K. Kim, J.H. Yoon, H.J. Moon, Association of preoperative US features and recurrence in patients with classic papillary thyroid carcinoma. Radiology 277, 574–583 (2015)

    Article  Google Scholar 

  37. J. Jonklaas, G. Nogueras-Gonzalez, M. Munsell, D. Litofsky, K. Ain, S. Bigos, J. Brierley, D.S. Cooper, B. Haugen, P.W. Ladenson, The impact of age and gender on papillary thyroid cancer survival. The Journal of Clinical Endocrinology & Metabolism 97, E878–E887 (2012)

    Article  CAS  Google Scholar 

  38. A. Toniato, I. Boschin, D. Casara, R. Mazzarotto, D. Rubello, M. Pelizzo, Papillary thyroid carcinoma: factors influencing recurrence and survival. Annals of Surgical Oncology 15, 1518–1522 (2008)

    Article  Google Scholar 

  39. G. Sapuppo, M. Tavarelli, A. Belfiore, R. Vigneri, G. Pellegriti, Response to Letter to the Editor: “Time to Separate Persistent From Recurrent Differentiated Thyroid Cancer: Different Conditions With Different Outcomes”, The Journal of Clinical Endocrinology & Metabolism 104, 5110–5111 (2019)

  40. A. Zahedi, L. Bondaz, M. Rajaraman, W.D. Leslie, C. Jefford, J.E. Young, K.A. Pathak, Y. Bureau, I. Rachinsky, M. Badreddine. Risk for Thyroid Cancer Recurrence Is Higher in Men Than in Women Independent of Disease Stage at Presentation. Thyroid: Official Journal of the American Thyroid Association. (2019)

  41. B.P. Pires, P.A.G. Alves Jr, M.A. Bordallo, D.A. Bulzico, F.P.P.L. Lopes, T. Farias, F. Dias, R.A. Lima, I.C. Santos Gisler, C.M. Coeli, Prognostic factors for early and long-term remission in pediatric differentiated thyroid carcinoma: the role of sex, age, clinical presentation, and the newly proposed American Thyroid Association risk stratification system. Thyroid: official journal of the American Thyroid Association 26, 1480–1487 (2016)

    Article  CAS  Google Scholar 

  42. R.M. Tuttle, H. Tala, J. Shah, R. Leboeuf, R. Ghossein, M. Gonen, M. Brokhin, G. Omry, J.A. Fagin, A. Shaha, Estimating risk of recurrence in differentiated thyroid cancer after total thyroidectomy and radioactive iodine remnant ablation: using response to therapy variables to modify the initial risk estimates predicted by the new American Thyroid Association staging system. Thyroid: official journal of the American Thyroid Association 20, 1341–1349 (2010)

    Article  CAS  Google Scholar 

  43. M.G. Castagna, F. Maino, C. Cipri, V. Belardini, A. Theodoropoulou, G. Cevenini, F. Pacini, Delayed risk stratification, to include the response to initial treatment (surgery and radioiodine ablation), has better outcome predictivity in differentiated thyroid cancer patients. European Journal of Endocrinology 165, 441 (2011)

    Article  CAS  Google Scholar 

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Author contributions

Concept and design: JQZ and ZWW. Acquisition of data: JWZ, YQH and ZYT. Analysis and interpretation of data: JWZ and MJF. Manuscript writing: JWZ and MJF. All the authors gave their final approval for the submission of this version and any revised version for publication.

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Author notes

  1. These authors contributed equally: Jing-Wen Zhang, Meng-Jia Fei

Authors and Affiliations

  1. Department of Ultrasound, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, China

    Jing-Wen Zhang, Yi-Qing Hou, Zhen-Yun Tang, Wei-Wei Zhan & Jian-Qiao Zhou

  2. Department of Head and Neck Surgery, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200001, China

    Meng-Jia Fei

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  1. Jing-Wen Zhang
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This study design was approved by the Ethics Committee of Ruijin Hospital, Shanghai Jiao Tong University School of Medicine and the need for informed consent was waived due to the retrospective analysis of this study.

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Zhang, JW., Fei, MJ., Hou, YQ. et al. Long-term follow-up ultrasonography surveillance in a large cohort of patients with papillary thyroid carcinoma. Endocrine 77, 297–304 (2022). https://doi.org/10.1007/s12020-022-03071-2

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  • DOI: https://doi.org/10.1007/s12020-022-03071-2

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