Skip to main content
Top
Published in: Endocrine 3/2017

01-03-2017 | Original Article

Chronic lymphocytic thyroiditis does not influence the risk of recurrence in patients with papillary thyroid carcinoma and excellent response to initial therapy

Authors: Marina S. Carvalho, Pedro W. Rosario, Gabriela F. Mourão, Maria R. Calsolari

Published in: Endocrine | Issue 3/2017

Login to get access

Abstract

Background

This study evaluated the recurrence in patients with papillary thyroid cancer and an excellent response to initial therapy, comparing those with and without chronic lymphocytic thyroiditis.

Methods

This was a prospective study. Patients who met the following criteria were selected: diagnosis of papillary thyroid cancer; submitted to total thyroidectomy followed or not by ablation with 131I; and neck ultrasonography without abnormalities, nonstimulated thyroglobulina (Tg) ≤0.2 ng/ml, and undetectable antithyroglobulin antibodies (TgAb) 12–18 months after initial therapy. The patients were divided into two groups: group A, with chronic lymphocytic thyroiditis on histology; group B, without chronic lymphocytic thyroiditis on histology.

Results

Groups A and B were similar in terms of sex and age of the patients, characteristics of the tumor, tumor-node-metastase stage and risk category. The time of follow-up ranged from 24 to 120 months (median 66 months). During follow-up, 5 patients of group A (2.6 %) and 9 patients of group B (2 %) developed recurrence (p = 0.77). Patients with chronic lymphocytic thyroiditis were more likely to progress to persistently borderline TgAb. No patient had positive TgAb (above the reference value) during follow-up. Recurrences occurred in 12/588 patients (2 %) with undetectable TgAb in all measurements, in 1/32 (3.1 %) with detectable TgAb on some occasion but that returned to undetectable spontaneously, and in 1/13 (7.7 %) with persistently borderline TgAb. These rates did not differ significantly (p = 0.25).

Conclusion

The results of the present study showed the absence of an association between chronic lymphocytic thyroiditis and recurrence risk at least in patients with an excellent response to initial therapy.
Literature
1.
go back to reference K. Kashima, S. Yokoyama, S. Noguchi, N. Murakami, H. Yamashita, S. Watanabe, S. Uchino, M. Toda, A. Sasaki, T. Daa, I. Nakayama, I. Chronic thyroiditis as a favorable prognostic factor in papillary thyroid carcinoma. Thyroid 8, 197–202 (1998)CrossRefPubMed K. Kashima, S. Yokoyama, S. Noguchi, N. Murakami, H. Yamashita, S. Watanabe, S. Uchino, M. Toda, A. Sasaki, T. Daa, I. Nakayama, I. Chronic thyroiditis as a favorable prognostic factor in papillary thyroid carcinoma. Thyroid 8, 197–202 (1998)CrossRefPubMed
2.
go back to reference K.C. Loh, F.S. Greenspan, F. Dong, T.R. Miller, P.P. Yeo, Influence of lymphocytic thyroiditis on the prognostic outcome of patients with papillary thyroid carcinoma. J. Clin. Endocrinol. Metab. 84, 458–463 (1999)CrossRefPubMed K.C. Loh, F.S. Greenspan, F. Dong, T.R. Miller, P.P. Yeo, Influence of lymphocytic thyroiditis on the prognostic outcome of patients with papillary thyroid carcinoma. J. Clin. Endocrinol. Metab. 84, 458–463 (1999)CrossRefPubMed
3.
go back to reference E. Kebebew, P.A. Treseler, P.H. Ituarte, O.H. Clark, Coexisting chronic lymphocytic thyroiditis and papillary thyroid cancer revisited. World. J. Surg. 25, 632–637 (2001)CrossRefPubMed E. Kebebew, P.A. Treseler, P.H. Ituarte, O.H. Clark, Coexisting chronic lymphocytic thyroiditis and papillary thyroid cancer revisited. World. J. Surg. 25, 632–637 (2001)CrossRefPubMed
4.
go back to reference E.Y. Kim, W.G. Kim, W.B. Kim, T.Y. Kim, J.M. Kim, J.S. Ryu, S.J. Hong, G. Gong, Y.K. Shong, Coexistence of chronic lymphocytic thyroiditis is associated with lower recurrence rates in patients with papillary thyroid carcinoma. Clin. Endocrinol. (Oxf) 71, 581–586 (2009)CrossRef E.Y. Kim, W.G. Kim, W.B. Kim, T.Y. Kim, J.M. Kim, J.S. Ryu, S.J. Hong, G. Gong, Y.K. Shong, Coexistence of chronic lymphocytic thyroiditis is associated with lower recurrence rates in patients with papillary thyroid carcinoma. Clin. Endocrinol. (Oxf) 71, 581–586 (2009)CrossRef
5.
go back to reference B.Y. Huang, C. Hseuh, T.C. Chao, K.J. Lin, J.D. Lin, Well-differentiated thyroid carcinoma with concomitant Hashimoto’s thyroiditis present with less aggressive clinical stage and low recurrence. Endocr. Pathol. 22, 144–149 (2011)CrossRefPubMed B.Y. Huang, C. Hseuh, T.C. Chao, K.J. Lin, J.D. Lin, Well-differentiated thyroid carcinoma with concomitant Hashimoto’s thyroiditis present with less aggressive clinical stage and low recurrence. Endocr. Pathol. 22, 144–149 (2011)CrossRefPubMed
6.
go back to reference J.S. Jeong, H.K. Kim, C.R. Lee, S. Park, J.H. Park, S.W. Kang, J.J. Jeong, K.H. Nam, W.Y. Chung, C.S. Park, Coexistence of chronic lymphocytic thyroiditis with papillary thyroid carcinoma: clinical manifestation and prognostic outcome. J. Korean Med. Sci. 27, 883–889 (2012)CrossRefPubMedPubMedCentral J.S. Jeong, H.K. Kim, C.R. Lee, S. Park, J.H. Park, S.W. Kang, J.J. Jeong, K.H. Nam, W.Y. Chung, C.S. Park, Coexistence of chronic lymphocytic thyroiditis with papillary thyroid carcinoma: clinical manifestation and prognostic outcome. J. Korean Med. Sci. 27, 883–889 (2012)CrossRefPubMedPubMedCentral
7.
go back to reference 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, 1341–1349 (2010)CrossRefPubMedPubMedCentral 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, 1341–1349 (2010)CrossRefPubMedPubMedCentral
8.
go back to reference 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. Eur. J. Endocrinol. 165, 441–446 (2011)CrossRefPubMed 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. Eur. J. Endocrinol. 165, 441–446 (2011)CrossRefPubMed
9.
go back to reference 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. (Oxf). 77, 132–138 (2012)CrossRefPubMed 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. (Oxf). 77, 132–138 (2012)CrossRefPubMed
10.
go back to reference M.J. Jeon, W.G. Kim, W.R. Park, J.M. Han, T.Y. Kim, D.E. Song, K.W. Chung, J.S. Ryu, S.J. Hong, Y.K. Shong, W.B. Kim, Modified dynamic risk stratification for predicting recurrence using the response to initial therapy in patients with differentiated thyroid carcinoma. Eur. J. Endocrinol. 170, 23–30 (2013)CrossRefPubMed M.J. Jeon, W.G. Kim, W.R. Park, J.M. Han, T.Y. Kim, D.E. Song, K.W. Chung, J.S. Ryu, S.J. Hong, Y.K. Shong, W.B. Kim, Modified dynamic risk stratification for predicting recurrence using the response to initial therapy in patients with differentiated thyroid carcinoma. Eur. J. Endocrinol. 170, 23–30 (2013)CrossRefPubMed
11.
go back to reference F. Pitoia, F. Bueno, C. Urciuoli, E. Abelleira, G. Cross, R.M. Tuttle, Outcomes of patients with differentiated thyroid cancer risk-stratified according to the American thyroid association and Latin American thyroid society risk of recurrence classification systems. Thyroid 23, 1401–1407 (2013)CrossRefPubMed F. Pitoia, F. Bueno, C. Urciuoli, E. Abelleira, G. Cross, R.M. Tuttle, Outcomes of patients with differentiated thyroid cancer risk-stratified according to the American thyroid association and Latin American thyroid society risk of recurrence classification systems. Thyroid 23, 1401–1407 (2013)CrossRefPubMed
12.
go back to reference R.S. Scheffel, A.B. Zanella, D. Antunes, J.M. Dora, A.L. Maia, Low recurrence rates in a cohort of differentiated thyroid carcinoma patients: a referral center experience. Thyroid 25, 883–889 (2015)CrossRefPubMed R.S. Scheffel, A.B. Zanella, D. Antunes, J.M. Dora, A.L. Maia, Low recurrence rates in a cohort of differentiated thyroid carcinoma patients: a referral center experience. Thyroid 25, 883–889 (2015)CrossRefPubMed
13.
go back to reference L. Giovanella, G. Treglia, R. Sadeghi, P. Trimboli, L. Ceriani, F.A. Verburg FA., Unstimulated highly sensitive thyroglobulin in follow-up of differentiated thyroid cancer patients: a meta-analysis. J. Clin. Endocrinol. Metab. 99, 440–447 (2014)CrossRefPubMed L. Giovanella, G. Treglia, R. Sadeghi, P. Trimboli, L. Ceriani, F.A. Verburg FA., Unstimulated highly sensitive thyroglobulin in follow-up of differentiated thyroid cancer patients: a meta-analysis. J. Clin. Endocrinol. Metab. 99, 440–447 (2014)CrossRefPubMed
14.
go back to reference M. Brassard, I. Borget, A. Edet-Sanson, A.L. Giraudet, O. Mundler, M. Toubeau, F. Bonichon, F. Borson-Chazot, L. Leenhardt, C. Schvartz, C. Dejax, I. Brenot-Rossi, M.E. Toubert, M. Torlontano, E. Benhamou, M. Schlumberger, Long-term follow-up of patients with papillary and follicular thyroid cancer: a prospective study on 715 patients. J. Clin. Endocrinol. Metab. 96, 1352–1359 (2011)CrossRefPubMed M. Brassard, I. Borget, A. Edet-Sanson, A.L. Giraudet, O. Mundler, M. Toubeau, F. Bonichon, F. Borson-Chazot, L. Leenhardt, C. Schvartz, C. Dejax, I. Brenot-Rossi, M.E. Toubert, M. Torlontano, E. Benhamou, M. Schlumberger, Long-term follow-up of patients with papillary and follicular thyroid cancer: a prospective study on 715 patients. J. Clin. Endocrinol. Metab. 96, 1352–1359 (2011)CrossRefPubMed
15.
go back to reference 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)CrossRefPubMedPubMedCentral 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)CrossRefPubMedPubMedCentral
16.
go back to reference P.W. Rosario, G.C. Penna, M.R. Calsolari, Noninvasive encapsulated follicular variant of papillary thyroid carcinoma: is lobectomy sufficient for tumours ≥1 cm? Clin Endocrinol. (Oxf) 81, 630–632 (2014)CrossRef P.W. Rosario, G.C. Penna, M.R. Calsolari, Noninvasive encapsulated follicular variant of papillary thyroid carcinoma: is lobectomy sufficient for tumours ≥1 cm? Clin Endocrinol. (Oxf) 81, 630–632 (2014)CrossRef
17.
go back to reference P.W. Rosario, S. de Faria, L. Bicalho, M.F. Alves, M.A. Borges, S. Purisch, E.L. Padrão, L.L. Rezende, A.L. Barroso, Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J. Ultrasound. Med. 24, 1385–1389 (2005)CrossRefPubMed P.W. Rosario, S. de Faria, L. Bicalho, M.F. Alves, M.A. Borges, S. Purisch, E.L. Padrão, L.L. Rezende, A.L. Barroso, Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J. Ultrasound. Med. 24, 1385–1389 (2005)CrossRefPubMed
18.
go back to reference P.W. Rosario, W.C. Tavares, M.A. Borges, J.B. Santos, M.R. Calsolari, Ultrasonographic differentiation of cervical lymph nodes in patients with papillary thyroid carcinoma after thyroidectomy and radioiodine ablation: a prospective study. Endocr. Pract. 20, 293–298 (2014)CrossRefPubMed P.W. Rosario, W.C. Tavares, M.A. Borges, J.B. Santos, M.R. Calsolari, Ultrasonographic differentiation of cervical lymph nodes in patients with papillary thyroid carcinoma after thyroidectomy and radioiodine ablation: a prospective study. Endocr. Pract. 20, 293–298 (2014)CrossRefPubMed
19.
go back to reference C. Durante, T. Montesano, M. Torlontano, M. Attard, F. Monzani, S. Tumino, G. Costante, D. Meringolo, R. Bruno, F. Trulli, M. Massa, A. Maniglia, R. D’Apollo, L. Giacomelli, G. Ronga, S. Filetti, Papillary thyroid cancer: time course of recurrences during postsurgery surveillance. J. Clin. Endocrinol. Metab. 98, 636–642 (2013)CrossRefPubMed C. Durante, T. Montesano, M. Torlontano, M. Attard, F. Monzani, S. Tumino, G. Costante, D. Meringolo, R. Bruno, F. Trulli, M. Massa, A. Maniglia, R. D’Apollo, L. Giacomelli, G. Ronga, S. Filetti, Papillary thyroid cancer: time course of recurrences during postsurgery surveillance. J. Clin. Endocrinol. Metab. 98, 636–642 (2013)CrossRefPubMed
20.
go back to reference F. Latrofa, D. Ricci, L. Montanelli, R. Rocchi, P. Piaggi, E. Sisti, L. Grasso, F. Basolo, C. Ugolini, A. Pinchera, P. Vitti, Lymphocytic thyroiditis on histology correlates with serum thyroglobulin autoantibodies in patients with papillary thyroid carcinoma: impact on detection of serum thyroglobulin. J. Clin. Endocrinol. Metab. 97, 2380–2387 (2012)CrossRefPubMed F. Latrofa, D. Ricci, L. Montanelli, R. Rocchi, P. Piaggi, E. Sisti, L. Grasso, F. Basolo, C. Ugolini, A. Pinchera, P. Vitti, Lymphocytic thyroiditis on histology correlates with serum thyroglobulin autoantibodies in patients with papillary thyroid carcinoma: impact on detection of serum thyroglobulin. J. Clin. Endocrinol. Metab. 97, 2380–2387 (2012)CrossRefPubMed
21.
go back to reference J.K. Chung, Y.J. Park, T.Y. Kim, Y. So, S.K. Kim, D.J. Park, D.S. Lee, M.C. Lee, B.Y. Cho, Clinical significance of elevated level of serum antithyroglobulin antibody in patients with differentiated thyroid cancer after thyroid ablation. Clin Endocrinol (Oxf) 57, 215–221 (2002)CrossRef J.K. Chung, Y.J. Park, T.Y. Kim, Y. So, S.K. Kim, D.J. Park, D.S. Lee, M.C. Lee, B.Y. Cho, Clinical significance of elevated level of serum antithyroglobulin antibody in patients with differentiated thyroid cancer after thyroid ablation. Clin Endocrinol (Oxf) 57, 215–221 (2002)CrossRef
22.
go back to reference W.G. Kim, J.H. Yoon, W.B. Kim, T.Y. Kim, E.Y. Kim, J.M. Kim, J.S. Ryu, G. Gong, S.J. Hong, Y.K. Shong, Change of serum antithyroglobulin antibody levels is useful for prediction of clinical recurrence in thyroglobulin-negative patients with differentiated thyroid carcinoma. J. Clin. Endocrinol. Metab. 93, 4683–4689 (2008)CrossRefPubMed W.G. Kim, J.H. Yoon, W.B. Kim, T.Y. Kim, E.Y. Kim, J.M. Kim, J.S. Ryu, G. Gong, S.J. Hong, Y.K. Shong, Change of serum antithyroglobulin antibody levels is useful for prediction of clinical recurrence in thyroglobulin-negative patients with differentiated thyroid carcinoma. J. Clin. Endocrinol. Metab. 93, 4683–4689 (2008)CrossRefPubMed
23.
go back to reference C.J. Hsieh, P.W. Wang, Sequential changes of serum antithyroglobulin antibody levels are a good predictor of disease activity in thyroglobulin-negative patients with papillary thyroid carcinoma. Thyroid 24, 488–493 (2014)CrossRefPubMed C.J. Hsieh, P.W. Wang, Sequential changes of serum antithyroglobulin antibody levels are a good predictor of disease activity in thyroglobulin-negative patients with papillary thyroid carcinoma. Thyroid 24, 488–493 (2014)CrossRefPubMed
24.
go back to reference C. Durante, S. Tognini, T. Montesano, F. Orlandi, M. Torlontano, E. Puxeddu, M. Attard, G. Costante, S. Tumino, D. Meringolo, R. Bruno, F. Trulli, M. Toteda, A. Redler, G. Ronga, S. Filetti, F. Monzani, Clinical aggressiveness and long-term outcome in patients with papillary thyroid cancer and circulating anti-thyroglobulin autoantibodies. Thyroid 24, 1139–1145 (2014)CrossRefPubMedPubMedCentral C. Durante, S. Tognini, T. Montesano, F. Orlandi, M. Torlontano, E. Puxeddu, M. Attard, G. Costante, S. Tumino, D. Meringolo, R. Bruno, F. Trulli, M. Toteda, A. Redler, G. Ronga, S. Filetti, F. Monzani, Clinical aggressiveness and long-term outcome in patients with papillary thyroid cancer and circulating anti-thyroglobulin autoantibodies. Thyroid 24, 1139–1145 (2014)CrossRefPubMedPubMedCentral
25.
go back to reference P.W. Rosario, M. Carvalho, G.F. Mourão, M.R. Calsolari, Comparison of antithyroglobulin antibody concentrations before and after ablation with 131I as a predictor of structural disease in differentiated thyroid carcinoma patients with undetectable basal thyroglobulin and negative neck ultrasonography. Thyroid 26, 525–531 (2016)CrossRefPubMed P.W. Rosario, M. Carvalho, G.F. Mourão, M.R. Calsolari, Comparison of antithyroglobulin antibody concentrations before and after ablation with 131I as a predictor of structural disease in differentiated thyroid carcinoma patients with undetectable basal thyroglobulin and negative neck ultrasonography. Thyroid 26, 525–531 (2016)CrossRefPubMed
26.
go back to reference L.L. Cunha, M.A. Marcello, S. Nonogaki, E.C. Morari, F.A. Soares, J. Vassallo, L.S. Ward, CD8+ tumour-infiltrating lymphocytes and COX2 expression may predict relapse in differentiated thyroid cancer. Clin. Endocrinol. (Oxf) 83, 246–253 (2015)CrossRef L.L. Cunha, M.A. Marcello, S. Nonogaki, E.C. Morari, F.A. Soares, J. Vassallo, L.S. Ward, CD8+ tumour-infiltrating lymphocytes and COX2 expression may predict relapse in differentiated thyroid cancer. Clin. Endocrinol. (Oxf) 83, 246–253 (2015)CrossRef
27.
go back to reference J.H. Lee, Y. Kim, J.W. Choi, Y.S. Kim, The association between papillary thyroid carcinoma and histologically proven Hashimoto’s thyroiditis: a meta-analysis. Eur. J. Endocrinol. 168, 343–349 (2013)CrossRefPubMed J.H. Lee, Y. Kim, J.W. Choi, Y.S. Kim, The association between papillary thyroid carcinoma and histologically proven Hashimoto’s thyroiditis: a meta-analysis. Eur. J. Endocrinol. 168, 343–349 (2013)CrossRefPubMed
Metadata
Title
Chronic lymphocytic thyroiditis does not influence the risk of recurrence in patients with papillary thyroid carcinoma and excellent response to initial therapy
Authors
Marina S. Carvalho
Pedro W. Rosario
Gabriela F. Mourão
Maria R. Calsolari
Publication date
01-03-2017
Publisher
Springer US
Published in
Endocrine / Issue 3/2017
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-016-1185-1

Other articles of this Issue 3/2017

Endocrine 3/2017 Go to the issue