Skip to main content
Top
Published in: Endocrine 1/2024

Open Access 28-08-2023 | Original Article

Impact of lymphovascular invasion on otherwise low-risk papillary thyroid carcinomas: a retrospective and observational study

Authors: Francisca Marques Puga, Abir Al Ghuzlan, Dana M. Hartl, Mohamed-Amine Bani, Sophie Moog, Fabiana Pani, Ingrid Breuskin, Joanne Guerlain, Matthieu Faron, Desirée Denadreis, Eric Baudin, Julien Hadoux, Livia Lamartina

Published in: Endocrine | Issue 1/2024

Login to get access

Abstract

Purpose

Presence of venous vascular invasion is a criterion of intermediate risk of recurrence in papillary thyroid carcinoma (PTC). However, the presence and type of vascular invasion (lymphatic or venous) is often underreported and its impact on PTCs without other risk features remains unknown. The aim of this study was to evaluate the impact of both lymphatic and venous invasion on the risk of recurrence/persistence on otherwise low-risk PTCs.

Methods

Retrospective study including patients with otherwise low-risk PTCs but with vascular invasion, diagnosed between 2013 and 2019. The persistence/recurrence during the follow-up was evaluated. Pathology was reviewed to confirm the presence of lymphovascular invasion and determine the type of invasion.

Results

A total of 141 patients were included. Lymphovascular invasion was confirmed in 20.6%. After surgery, 48.9% (N = 69) of the patients received radioactive iodine (RAI). The median follow-up time was 4 [3–6] years. Overall, 6 (4.2%) patients experienced persistent/recurrent disease in the neck, including 3 with lymphovascular invasion, confirmed as “only lymphatic”. Overall, patients with tumors harboring lymphovascular invasion had sensibly more persistent/recurrence disease compared with those without lymphovascular invasion (10.3% vs 2.7%, p = 0.1), especially in the subgroup of patients not treated with RAI (20% vs 1.6%, p = 0.049) [OR 15.25, 95% CI 1.24-187.85, p = 0.033].

Conclusion

Lymphovascular invasion, including lymphatic invasion only, is associated with a sensibly higher risk of persistent/recurrent disease in otherwise low-risk PTCs, namely in patients not treated with RAI. Lymphatic invasion could have a role in risk-stratification systems for decision making.
Appendix
Available only for authorised users
Literature
1.
go back to reference L. Davies, H.G. Welch, Current thyroid cancer trends in the United States. JAMA Otolaryngol. Head. Neck Surg. 140, 317 (2014)CrossRefPubMed L. Davies, H.G. Welch, Current thyroid cancer trends in the United States. JAMA Otolaryngol. Head. Neck Surg. 140, 317 (2014)CrossRefPubMed
2.
go back to reference J.P. Brito, A. Al Nofal, V.M. Montori, I.D. Hay, J.C. Morris, The impact of subclinical disease and mechanism of detection on the rise in thyroid cancer incidence: a population-based study in olmsted county, minnesota during 1935 Through 2012. Thyroid 25, 999–1007 (2015)CrossRefPubMedPubMedCentral J.P. Brito, A. Al Nofal, V.M. Montori, I.D. Hay, J.C. Morris, The impact of subclinical disease and mechanism of detection on the rise in thyroid cancer incidence: a population-based study in olmsted county, minnesota during 1935 Through 2012. Thyroid 25, 999–1007 (2015)CrossRefPubMedPubMedCentral
3.
go back to reference B. Aschebrook-Kilfoy, M.H. Ward, M.M. Sabra, S.S. Devesa, Thyroid cancer incidence patterns in the United States by histologic type, 1992–2006. Thyroid 21, 125–134 (2011)CrossRefPubMedPubMedCentral B. Aschebrook-Kilfoy, M.H. Ward, M.M. Sabra, S.S. Devesa, Thyroid cancer incidence patterns in the United States by histologic type, 1992–2006. Thyroid 21, 125–134 (2011)CrossRefPubMedPubMedCentral
4.
go back to reference L. Leenhardt, M.O. Bernier, M.H. Boin-Pineau, B. Conte Devolx, R. Maréchaud, P. Niccoli-Sire, M. Nocaudie, J. Orgiazzi, M. Schlumberger, J.L. Wémeau, L. Chérie-Challine, F. De Vathaire, Advances in diagnostic practices affect thyroid cancer incidence in France. Eur. J. Endocrino. 133–139 (2004). L. Leenhardt, M.O. Bernier, M.H. Boin-Pineau, B. Conte Devolx, R. Maréchaud, P. Niccoli-Sire, M. Nocaudie, J. Orgiazzi, M. Schlumberger, J.L. Wémeau, L. Chérie-Challine, F. De Vathaire, Advances in diagnostic practices affect thyroid cancer incidence in France. Eur. J. Endocrino. 133–139 (2004).
5.
go back to reference S. Vaccarella, S. Franceschi, F. Bray, C.P. Wild, M. Plummer, Dal, L. Maso, Worldwide thyroid-cancer epidemic? The increasing impact of overdiagnosis. N. Engl. J. Med. 375, 614–617 (2016)CrossRefPubMed S. Vaccarella, S. Franceschi, F. Bray, C.P. Wild, M. Plummer, Dal, L. Maso, Worldwide thyroid-cancer epidemic? The increasing impact of overdiagnosis. N. Engl. J. Med. 375, 614–617 (2016)CrossRefPubMed
6.
go back to reference B.C. James, J.M. Mitchell, H.D. Jeon, N. Vasilottos, R.H. Grogan, B. Aschebrook-Kilfoy, An update in international trends in incidence rates of thyroid cancer, 1973–2007. Cancer Causes Control 29, 465–473 (2018)CrossRefPubMed B.C. James, J.M. Mitchell, H.D. Jeon, N. Vasilottos, R.H. Grogan, B. Aschebrook-Kilfoy, An update in international trends in incidence rates of thyroid cancer, 1973–2007. Cancer Causes Control 29, 465–473 (2018)CrossRefPubMed
7.
go back to reference A. Maniakas, L. Davies, M.E. Zafereo, Thyroid disease around the World. Otolaryngologic Clin. North Am. 51, 631–642 (2018)CrossRef A. Maniakas, L. Davies, M.E. Zafereo, Thyroid disease around the World. Otolaryngologic Clin. North Am. 51, 631–642 (2018)CrossRef
8.
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
9.
go back to reference L. Falvo, A. Catania, V. D’Andrea, A. Marzullo, M.C. Giustiniani, E. De Antoni, Prognostic importance of histologic vascular invasion in papillary thyroid carcinoma. Ann. Surg. 241, 640–646 (2005)CrossRefPubMedPubMedCentral L. Falvo, A. Catania, V. D’Andrea, A. Marzullo, M.C. Giustiniani, E. De Antoni, Prognostic importance of histologic vascular invasion in papillary thyroid carcinoma. Ann. Surg. 241, 640–646 (2005)CrossRefPubMedPubMedCentral
10.
go back to reference R.E. Gardner, R.M. Tuttle, K.D. Burman, S. Haddady, C. Truman, Y.H. Sparling, L. Wartofsky, R.B. Sessions, M.D. Ringel, Prognostic importance of vascular invasion in papillary thyroid carcinoma. Arch. Otolaryngol. Head. Neck Surg. 126, 309 (2000)CrossRefPubMed R.E. Gardner, R.M. Tuttle, K.D. Burman, S. Haddady, C. Truman, Y.H. Sparling, L. Wartofsky, R.B. Sessions, M.D. Ringel, Prognostic importance of vascular invasion in papillary thyroid carcinoma. Arch. Otolaryngol. Head. Neck Surg. 126, 309 (2000)CrossRefPubMed
11.
go back to reference O. Mete, S.L. Asa, Pathological definition and clinical significance of vascular invasion in thyroid carcinomas of follicular epithelial derivation. Mod. Pathol. 24, 1545–1552 (2011)CrossRefPubMed O. Mete, S.L. Asa, Pathological definition and clinical significance of vascular invasion in thyroid carcinomas of follicular epithelial derivation. Mod. Pathol. 24, 1545–1552 (2011)CrossRefPubMed
12.
go back to reference T. Nishida, S. Katayama, M. Tsujimoto, The clinicopathological significance of histologic vascular invasion in differentiated thyroid carcinoma. Am. J. Surg. 183, 80–86 (2002).CrossRefPubMed T. Nishida, S. Katayama, M. Tsujimoto, The clinicopathological significance of histologic vascular invasion in differentiated thyroid carcinoma. Am. J. Surg. 183, 80–86 (2002).CrossRefPubMed
13.
go back to reference L.A. Akslen, A.O. Myking, H. Salvesen, J.E. Varhaug, Prognostic importance of various clinicopathological features in papillary thyroid carcinoma. Eur. J. Cancer 29, 44–51 (1993)CrossRef L.A. Akslen, A.O. Myking, H. Salvesen, J.E. Varhaug, Prognostic importance of various clinicopathological features in papillary thyroid carcinoma. Eur. J. Cancer 29, 44–51 (1993)CrossRef
14.
go back to reference W.J. Simpson, S.E. McKinney, J.S. Carruthers, M.K. Gospodarowicz, S.B. Sutcliffe, T. Panzarella, Papillary and follicular thyroid cancer. Am. J. Med. 83, 479–488 (1987)CrossRefPubMed W.J. Simpson, S.E. McKinney, J.S. Carruthers, M.K. Gospodarowicz, S.B. Sutcliffe, T. Panzarella, Papillary and follicular thyroid cancer. Am. J. Med. 83, 479–488 (1987)CrossRefPubMed
15.
go back to reference K.T. Mai, P. Khanna, H.M. Yazdi, D.G. Perkins, J.P. Veinot, J. Thomas, M. Lamba, B.D. Nair, Differentiated thyroid carcinomas with vascular invasion: a comparative study of follicular, Hürthle cell and papillary thyroid carcinoma. Pathology 34(3), 239–244 (2002)CrossRefPubMed K.T. Mai, P. Khanna, H.M. Yazdi, D.G. Perkins, J.P. Veinot, J. Thomas, M. Lamba, B.D. Nair, Differentiated thyroid carcinomas with vascular invasion: a comparative study of follicular, Hürthle cell and papillary thyroid carcinoma. Pathology 34(3), 239–244 (2002)CrossRefPubMed
16.
go back to reference J.C. Furlan, Y.C. Bedard, I.B. Rosen, Clinicopathologic significance of histologic vascular invasion in papillary and follicular thyroid carcinomas1. J. Am. Coll. Surg. 198, 341–348 (2004)CrossRefPubMed J.C. Furlan, Y.C. Bedard, I.B. Rosen, Clinicopathologic significance of histologic vascular invasion in papillary and follicular thyroid carcinomas1. J. Am. Coll. Surg. 198, 341–348 (2004)CrossRefPubMed
17.
go back to reference L. Lamartina, S. Bidault, J. Hadoux, J. Guerlain, E. Girard, I. Breuskin, M. Attard, V. Suciu, E. Baudin, A. Al Ghuzlan, S. Leboulleux, D. Hartl, Can preoperative ultrasound predict extrathyroidal extension of differentiated thyroid cancer? Eur. J. Endocrinol. 185, 13–22 (2021)CrossRefPubMed L. Lamartina, S. Bidault, J. Hadoux, J. Guerlain, E. Girard, I. Breuskin, M. Attard, V. Suciu, E. Baudin, A. Al Ghuzlan, S. Leboulleux, D. Hartl, Can preoperative ultrasound predict extrathyroidal extension of differentiated thyroid cancer? Eur. J. Endocrinol. 185, 13–22 (2021)CrossRefPubMed
18.
go back to reference S. Bidault, E. Girard, M. Attard, G. Garcia, J. Guerlain, I. Breuskin, E. Baudin, J. Hadoux, C. Garcia, L. Lamartina, D.M. Hartl, Preoperative ultrasound mapping of the vagus nerve in thyroid surgery. Gland Surg. 11, 91–99 (2022)CrossRefPubMedPubMedCentral S. Bidault, E. Girard, M. Attard, G. Garcia, J. Guerlain, I. Breuskin, E. Baudin, J. Hadoux, C. Garcia, L. Lamartina, D.M. Hartl, Preoperative ultrasound mapping of the vagus nerve in thyroid surgery. Gland Surg. 11, 91–99 (2022)CrossRefPubMedPubMedCentral
20.
go back to reference C. Wittekind, TNM Klassifikation maligner Tumoren. (Springer, Berlin, 2020) C. Wittekind, TNM Klassifikation maligner Tumoren. (Springer, Berlin, 2020)
21.
go back to reference L. Lamartina, D. Handkiewicz-Junak, Follow-up of low risk thyroid cancer patients: can we stop follow-up after 5 years of complete remission? Eur. J. Endocrinol. 182, D1–D16 (2020)CrossRefPubMed L. Lamartina, D. Handkiewicz-Junak, Follow-up of low risk thyroid cancer patients: can we stop follow-up after 5 years of complete remission? Eur. J. Endocrinol. 182, D1–D16 (2020)CrossRefPubMed
22.
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; PTC Study Group, 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; PTC Study Group, Papillary thyroid cancer: time course of recurrences during postsurgery surveillance. J. Clin. Endocrinol. Metab. 98, 636–642 (2013)CrossRefPubMed
23.
go back to reference G. Grani, L. Lamartina, C. Durante, S. Filetti, D.S. Cooper, Follicular thyroid cancer and Hürthle cell carcinoma: challenges in diagnosis, treatment, and clinical management. Lancet Diabetes Endocrinol. 6, 500–514 (2018)CrossRefPubMed G. Grani, L. Lamartina, C. Durante, S. Filetti, D.S. Cooper, Follicular thyroid cancer and Hürthle cell carcinoma: challenges in diagnosis, treatment, and clinical management. Lancet Diabetes Endocrinol. 6, 500–514 (2018)CrossRefPubMed
24.
go back to reference S. Hescot, H. Sheikh-Alard, M. Kordahi, D. Hartl, J. Hadoux, M. Terroir, I. Breuskin, E. Baudin, J.Y. Scoazec, M. Schlumberger, A. Al Ghuzlan, S. Leboulleux, Impact of expert review of histological diagnosis of papillary and follicular thyroid cancer. Endocrine 72, 791–797 (2021)CrossRefPubMed S. Hescot, H. Sheikh-Alard, M. Kordahi, D. Hartl, J. Hadoux, M. Terroir, I. Breuskin, E. Baudin, J.Y. Scoazec, M. Schlumberger, A. Al Ghuzlan, S. Leboulleux, Impact of expert review of histological diagnosis of papillary and follicular thyroid cancer. Endocrine 72, 791–797 (2021)CrossRefPubMed
Metadata
Title
Impact of lymphovascular invasion on otherwise low-risk papillary thyroid carcinomas: a retrospective and observational study
Authors
Francisca Marques Puga
Abir Al Ghuzlan
Dana M. Hartl
Mohamed-Amine Bani
Sophie Moog
Fabiana Pani
Ingrid Breuskin
Joanne Guerlain
Matthieu Faron
Desirée Denadreis
Eric Baudin
Julien Hadoux
Livia Lamartina
Publication date
28-08-2023
Publisher
Springer US
Published in
Endocrine / Issue 1/2024
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-023-03475-8

Other articles of this Issue 1/2024

Endocrine 1/2024 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.