Abstract
Purpose
To investigate the role of neck US surveillance in patients with papillary thyroid carcinoma (PTC) after total thyroidectomy according to dynamic risk stratification (DRS) based on response to initial therapy.
Methods
This retrospective study included 812 patients with PTC who underwent total thyroidectomy with prophylactic central neck dissection from January 2003 through February 2007. The relative risk of recurrence/persistence according to DRS was evaluated with the multivariable Cox regression proportional hazard model.
Results
There were 132 men and 680 women. The mean age at surgery was 45.2 years. Postoperative US was used for DRS. According to DRS, 676 patients had excellent response, 78 indeterminate response, 40 biochemical incomplete response, and 18 structural incomplete response to initial therapy. Neck US was performed during follow-up and detected locoregional recurrences in 21 patients (2.6%): 12 with excellent response, 2 with biochemical incomplete response, and 7 with structural incomplete response according to DRS. Only 1 patient (0.1%) with excellent response had a locoregional recurrence that exceeded 8 mm in its shortest diameter, which is the size cut-off for diagnostic US fine-needle aspiration in suspicious lymph nodes. This patient did not develop biochemical abnormalities during follow-up.
Conclusions
Postoperative neck US surveillance after total thyroidectomy with prophylactic central neck dissection is not essential in PTC patients who show excellent response to initial therapy. Future studies are needed to verify the role of US surveillance in patients who receive variable degrees of treatments.
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Abbreviations
- LN:
-
lymph node
- PTC:
-
papillary thyroid carcinoma
- Tg:
-
thyroglobulin
- ATA:
-
American Thyroid Association
- FNA:
-
fine-needle aspiration
- DRS:
-
dynamic risk stratification
- RAI:
-
radioiodine ablation
- TSH:
-
thyroid-stimulating hormone
- DFS:
-
disease free survival
References
P.L. Horn-Ross, D.Y. Lichtensztajn, C.A. Clarke, C. Dosiou, I. Oakley-Girvan, P. Reynolds, S.L. Gomez, D.O. Nelson, Continued rapid increase in thyroid cancer incidence in california: trends by patient, tumor, and neighborhood characteristics. Cancer Epidemiol. Biomarkers Prev. 23(6), 1067–1079 (2014)
National Cancer Institute. Surveillance, epidemiology, and end results program. https://seer.cancer.gov/. Accessed 7 July 2019
S. Zuniga, A. Sanabria, Prophylactic central neck dissection in stage N0 papillary thyroid carcinoma. Arch. Otolaryngol. Head Neck Surg. 135(11), 1087–1091 (2009)
S. Noguchi, A. Noguchi, N. Murakami, Papillary carcinoma of the thyroid. I. Developing pattern of metastasis. Cancer 26(5), 1053–1060 (1970)
S. Noguchi, A. Noguchi, N. Murakami, Papillary carcinoma of the thyroid. II. Value of prophylactic lymph node excision. Cancer 26(5), 1061–1064 (1970)
N. Wada, Q.Y. Duh, K. Sugino, H. Iwasaki, K. Kameyama, T. Mimura, K. Ito, H. Takami, Y. Takanashi, Lymph node metastasis from 259 papillary thyroid microcarcinomas: frequency, pattern of occurrence and recurrence, and optimal strategy for neck dissection. Ann. Surg. 237(3), 399–407 (2003)
R.M. Tuttle, R. Leboeuf, A.J. Martorella, Papillary thyroid cancer: monitoring and therapy. Endocrinol. Metab. Clin. North Am. 36(3), 753–778 (2007).
A. Stojadinovic, M. Shoup, A. Nissan, R.A. Ghossein, J.P. Shah, M.F. Brennan, A.R. Shaha, Recurrent differentiated thyroid carcinoma: biological implications of age, method of detection, and site and extent of recurrence. Ann. Surg. Oncol. 9(8), 789–798 (2002)
E.L. Mazzaferri, R.T. Kloos, Clinical review 128: current approaches to primary therapy for papillary and follicular thyroid cancer. J. Clin. Endocrinol. Metab. 86(4), 1447–1463 (2001)
F. Pacini, E. Molinaro, M.G. 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. J. Clin. Endocrinol. Metab. 88(8), 3668–3673 (2003)
A. Antonelli, P. Miccoli, M. Ferdeghini, G. Di Coscio, B. Alberti, P. Iacconi, V. Baldi, P. Fallahi, L. Baschieri, Role of neck ultrasonography in the follow-up of patients operated on for thyroid cancer. Thyroid 5(1), 25–28 (1995)
A. Frasoldati, M. Pesenti, M. Gallo, A. Caroggio, D. Salvo, R. Valcavi, Diagnosis of neck recurrences in patients with differentiated thyroid carcinoma. Cancer 97(1), 90–96 (2003)
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), 1–133 (2016)
M. Banerjee, J.L. Wiebel, C. Guo, B. Gay, M.R. Haymart, Use of imaging tests after primary treatment of thyroid cancer in the United States: population based retrospective cohort study evaluating death and recurrence. BMJ 354, i3839 (2016)
J.H. Yoon, H.S. Lee, E.K. Kim, J.H. Youk, H.G. Kim, H.J. Moon, J.Y. Kwak, Short-term follow-up US leads to higher false-positive results without detection of structural recurrences in PTMC. Medicine 95(1), e2435 (2016)
S. Epstein, R. McEachern, R. Khot, S. Padia, J.T. Patrie, J.N. Itri, Papillary thyroid carcinoma recurrence: low yield of neck ultrasound with an undetectable serum thyroglobulin level. J. Ultrasound Med. 37(10), 2325–2331 (2018)
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, K.J. Ahn, H.S. Ahn, H.J. Baek, Utility of routine ultrasonography follow-up after total thyroidectomy in patients with papillary thyroid carcinoma: a single-center study. BMC Med. Imaging 18(1), 12 (2018)
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 Radiol. 59(2), 196–203 (2018)
G. Grani, V. Ramundo, R. Falcone, L. Lamartina, T. Montesano, M. Biffoni, L. Giacomelli, M. Sponziello, A. Verrienti, M. Schlumberger, S. Filetti, C. Durante, Thyroid cancer patients with no evidence of disease: the need for repeat neck ultrasound. J. Clin. Endocrinol. Metab. 104(11), 4981–4989 (2019)
K. Kim, J.H. Kim, I.S. Park, Y.S. Rho, G.H. Kwon, D.J. Lee, The updated AJCC/TNM staging system for papillary thyroid cancer (8th Edition): from the perspective of genomic analysis. World J. Surg. (2018). https://doi.org/10.1007/s00268-018-4662-2
M.J. Kim, E.K. Kim, B.M. Kim, J.Y. Kwak, E.J. Lee, C.S. Park, W.Y. Cheong, K.H. Nam, Thyroglobulin measurement in fine-needle aspirate washouts: the criteria for neck node dissection for patients with thyroid cancer. Clin. Endocrinol. 70(1), 145–151 (2009)
D.W. Kim, H.J. Choo, Y.J. Lee, S.J. Jung, J.W. Eom, T.K. Ha, Sonographic features of cervical lymph nodes after thyroidectomy for papillary thyroid carcinoma. J. Ultrasound Med. 32(7), 1173–1180 (2013)
K. Bibbins-Domingo, D.C. Grossman, S.J. Curry, M.J. Barry, K.W. Davidson, C.A. Doubeni, J.W. Epling Jr., A.R. Kemper, A.H. Krist, A.E. Kurth, C.S. Landefeld, C.M. Mangione, M.G. Phipps, M. Silverstein, M.A. Simon, A.L. Siu, C.W. Tseng, Screening for thyroid cancer: US preventive services task force recommendation statement. JAMA 317(18), 1882–1887 (2017)
L. Lamartina, G. Grani, C. Durante, I. Borget, S. Filetti, M. Schlumberger, Follow-up of differentiated thyroid cancer—what should (and what should not) be done. Nat. Rev. Endocrinol. 14(9), 538–551 (2018)
L.Y. Wang, B.R. Roman, J.C. Migliacci, F.L. Palmer, R.M. Tuttle, A.R. Shaha, J.P. Shah, S.G. Patel, I. Ganly, Cost-effectiveness analysis of papillary thyroid cancer surveillance. Cancer 121(23), 4132–4140 (2015)
J.L. Gray, G. Singh, L. Uttley, S.P. Balasubramanian, Routine thyroglobulin, neck ultrasound and physical examination in the routine follow up of patients with differentiated thyroid cancer—where is the evidence? Endocrine 62(1), 26–33 (2018)
E. Baudin, C. Do Cao, A.F. Cailleux, S. Leboulleux, J.P. Travagli, M. Schlumberger, Positive predictive value of serum thyroglobulin levels, measured during the first year of follow-up after thyroid hormone withdrawal, in thyroid cancer patients. J. Clin. Endocrinol. Metab. 88(3), 1107–1111 (2003)
M. Schlumberger, S. Leboulleux, B. Catargi, D. Deandreis, S. Zerdoud, S. Bardet, D. Rusu, Y. Godbert, C. Buffet, C. Schvartz, P. Vera, O. Morel, D. Benisvy, C. Bournaud, M.-E. Toubert, A. Kelly, E. Benhamou, I. Borget, Outcome after ablation in patients with low-risk thyroid cancer (ESTIMABL1): 5-year follow-up results of a randomised, phase 3, equivalence trial. Lancet Diabetes Endocrinol. 6(8), 618–626 (2018)
S. Leboulleux, I. Borget, M. Schlumberger, Radioactive iodine ablation in low-risk thyroid cancer—authors’ reply. Lancet Diabetes Endocrinol. 6(9), 686–687 (2018)
C. Durante, T. Montesano, M. Attard, M. Torlontano, F. Monzani, G. Costante, D. Meringolo, M. Ferdeghini, S. Tumino, L. Lamartina, A. Paciaroni, M. Massa, L. Giacomelli, G. Ronga, S. Filetti, Long-term surveillance of papillary thyroid cancer patients who do not undergo postoperative radioiodine remnant ablation: is there a role for serum thyroglobulin measurement? J. Clin. Endocrinol. Metab. 97(8), 2748–2753 (2012)
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 20(12), 1341–1349 (2010)
F. Vaisman, D. Momesso, D.A. Bulzico, C.H. Pessoa, F. Dias, R. Corbo, M. Vaisman, R.M. Tuttle, Spontaneous remission in thyroid cancer patients after biochemical incomplete response to initial therapy. Clin. Endocrinol. 77(1), 132–138 (2012).
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Yoon, J., Yoon, J.H., Han, K. et al. Ultrasonography surveillance in papillary thyroid carcinoma patients after total thyroidectomy according to dynamic risk stratification. Endocrine 69, 347–357 (2020). https://doi.org/10.1007/s12020-020-02347-9
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DOI: https://doi.org/10.1007/s12020-020-02347-9