Abstract
Purpose
Lymphadenectomy in papillary thyroid carcinoma (PTC) continues to be controversial. A better staging method is needed to provide adequate individual surgical treatment. SPECT/CT lymphoscintigraphy and sentinel lymph node (SLN) biopsy may improve lymphatic staging and surgical treatment. Our main objectives were to describe the lymphatic drainage of PTC using lymphoscintigraphy, to evaluate the lymphatic spread (comparing SLN and lymphadenectomy results) and to analyse the impact of SLN identification in surgery.
Methods
We prospectively studied 24 consecutive patients with PTC (19 women; mean age 52.7 years, range 22–81 years). The day before surgery, lymphoscintigraphy with ultrasound-guided intratumoral injection (99mTc-nanocolloid, 148 MBq) was performed, obtaining planar and SPECT/CT images. All patients underwent total thyroidectomy, SLN biopsy (hand-held gamma probe) with perioperative analysis, central compartment node dissection, or laterocervical lymphadenectomy if perioperative stage N1b or positive SLNs in this lymphatic basin.
Results
Lymphoscintigraphy revealed at least one SLN in 19 of 24 patients (79 %) on planar and SPECT/CT images, and in 23 of 24 patients (96 %) during surgery using a hand-held gamma probe. Lymph node metastases were detected with classical perioperative techniques (ultrasound guidance and surgical inspection) in 3 of 24 patients, by perioperative SLN analysis in 10 of 23, and by definitive histology in 13 of 24. The false-negative (FN) ratio for SLN was 7.7 % (one patient with bulky lymph nodes). The FN ratio for perioperative frozen sections was 15.4 % (two patients, one with micrometastases, the other with bilateral SLN). Lymphatic drainage was only to the central compartment in 6 of 24 patients (3 of the 6 with positive SLNs for metastases), only to the laterocervical basin in 5 of 24 patients (all unilateral, 2 of 5 positive SLNs) and to the central and laterocervical compartments in 12 of 24 patients (6 of 12 and 3 of 12 positive SLNs, respectively).
Conclusion
Lymphoscintigraphy reveals the lymph node drainage in a high proportion of patients. It detects laterocervical drainage in a significant percentage of patients, allowing the detection of occult lymph node metastases and improving the surgical management in PTC.
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References
Hundahl S, Fleming I, Fremgen A, Menck H. A National Center Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985–1995. Cancer. 1998;83:2638–48.
American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer; Cooper D, Doherty G, Haugen B, Kloos RT, Lee SL, Mandel SJ, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009;19:1167–214.
Dralle H, Machens A. Surgical approaches in thyroid cancer and lymph-node metastases. Best Pract Res Clin Endocrinol Metab. 2008;22:971–87.
Carling T, Long 3rd WD, Udelsman R. Controversy surrounding the role for routine central lymph node dissection for differentiated thyroid cancer. Curr Opin Oncol. 2010;22:30–4.
Lundgren CI, Hall P, Dickman PW, Zedenius J. Clinically significant prognostic factors for differentiated thyroid carcinoma: a population-based, nested case-control study. Cancer. 2006;106(3):524–31.
Mazzaferri E, Doherty G, Steward D. The pros and cons of prophylactic central compartment lymph node dissection for papillary thyroid carcinoma. Thyroid. 2009;19:683–9.
Sakorafas G, Sampanis D, Safioleas M. Cervical lymph node dissection in papillary thyroid cancer: current trends, persisting controversies, and unclarified uncertainties. Surg Oncol. 2010;19:e58–70.
Cheng G, Kurita S, Torigian D, Alavi A. Current status of sentinel lymph-node biopsy in patients with breast cancer. Eur J Nucl Med Mol Imaging. 2011;38:562–75.
Prieto V. Sentinel lymph nodes in cutaneous melanoma. Clin Lab Med. 2011;31:301–10.
Kelemen P, Van Herle A, Giuliano A. Sentinel lymphadenectomy in thyroid malignant neoplasms. Arch Surg. 1998;133:288–92.
Rubello D, Pelizzo M, Al-Nahhas A, Salvatori M, O'Doherty MJ, Giuliano AE, et al. The role of sentinel lymph node biopsy in patients with differentiated thyroid carcinoma. Eur J Surg Oncol. 2006;32:917–21.
Anand S, Gologan O, Rochon L, Tamilia M, How J, Hier MP, et al. The role of sentinel lymph node biopsy in differentiated thyroid carcinoma. Arch Otolaryngol Head Neck Surg. 2009;135:1199–204.
Dixon E, McKinnon J, Pasieka J. Feasibility of sentinel lymph node biopsy and lymphatic mapping in nodular thyroid neoplasms. World J Surg. 2000;24:1396–401.
Rettenbacher L, Sungler P, Gmeiner D, Kässmann H, Galvan G. Detecting the sentinel lymph node in patients with differentiated thyroid carcinoma. Eur J Nucl Med. 2000;27:1399–401.
Sahin M, Yapici O, Dervisoglu A, Basoglu T, Canbaz F, Albayrak S, et al. Evaluation of lymphatic drainage of cold thyroid nodules with intratumoral injection of Tc-99m nanocolloid. Clin Nucl Med. 2001;26:602–5.
Catarci M, Zaraca F, Angeloni R, Mancini B, de Filippo MG, Massa R, et al. Preoperative lymphoscintigraphy and sentinel lymph node biopsy in papillary thyroid cancer. A pilot study. J Surg Oncol. 2001;77:21–4.
Tsugawa K, Noguchi M, Miwa K, Bando E, Yokoyama K, Nakajima K, et al. Dye- and gamma probe-guided sentinel lymph node biopsy in breast cancer patients: using patent blue dye and technetium-99m-labeled human serum albumin. Breast Cancer. 2000;7:87–94.
Fukui Y, Yamakawa T, Taniki T, Numoto S, Miki H, Monden Y. Sentinel lymph node biopsy in patients with papillary thyroid carcinoma. Cancer. 2001;92:2868–74.
Arch J, Velasquez D, Fajardo R, Gamboa A, Herrera M. Accuracy of sentinel lymph node in papillary thyroid carcinoma. Surgery. 2001;130(6):907–13.
Pellizo M, Boschi I, Toniato A, Bernante P, Piotto A, Rinaldo A, et al. The sentinel node procedure with Patent Blue V dye in the surgical treatment of papillary thyroid carcinoma. Acta Otolaryngol. 2001;121(3):421–4.
Stoeckli S, Pfaltz Steiner H, Schmid S. Sentinel lymph node biopsy in thyroid tumors: a pilot study. Eur Arch Otorhinolaryngol. 2003;260:364–8.
Takami H, Sasaki K, Ikeda Y, Tajima G, Kameyama K. Detection of sentinel lymph nodes in patients with papillary thyroid cancer. Asian J Surg. 2003;26:145–8.
Dzodic R, Markovic I, Inic M, Jokic N, Zegarac M, Djurisic I, et al. Identification of sentinel lymph in thyroid carcinoma. Acta Chir Iugosl. 2003;50:103–6.
Chow T, Lim B, Kwok S. Sentinel lymph node dissection in papillary thyroid carcinoma. ANZ J Surg. 2004;74:10–2.
Nakano S, Uenosono Y, Ehi K, Arigami T, Higashi Y, Maeda T, et al. Lymph node mapping for detection of sentinel nodes in patients with papillary thyroid cancer. Gan To Kagaku Ryoho. 2004;31:801–4.
Peparini N, Maturo A, Di Matteo F, Tartaglia F, Marchesi M, Campana E. Blue-dye sentinel node mapping in thyroid carcinoma: debatable results of feasibility. Acta Chir Bel. 2006;32:523–7.
Pellizo M, Merante I, Toniato A, Piotto A, Bernante P, Paggetta C, et al. Sentinel node mapping and biopsy in thyroid cancer: a surgical perspective. Biomed Pharmacother. 2006;60(8):4405–8.
Dzodic R, Markovic I, Inic M, Jokic N, Djurisic I, Zegarac M, et al. Sentinel lymph node biopsy may be used to support the decision to perform modified radical neck dissection in differentiated thyroid carcinoma. World J Surg. 2006;30(5):841–6.
Pellizo M, Merante I, Piotto A, Bernante P, Pagetta C, Rubello D, et al. Sentinel lymph node procedure in thyroid carcinoma patients. Our experience. Minerva Chir. 2006;61(1):25–9.
Rubello D, Nanni C, Merante I, Toniato A, Piotto A, Rampin A, et al. Sentinel lymph node (SLN) procedure with patent V blue dye in 153 patients with papillary thyroid carcinoma (PTC): is it an accurate staging method? J Exp Clin Cancer Res. 2006;25(4):483–6.
Nenkov R, Radev R, Madzhov R, Krasnaliev I. Sentinel lymph node biopsy in patients with papillary thyroid carcinoma. Khirurgiia (Sofiia). 2006;(6):55–6.
Carcoforo P, Feggi L, Transforini G, Lanzara S, Sortini D, Zulian V, et al. Use of preoperative lymphoscintigraphy and intraoperative gamma-probe detection for identification of the sentinel lymph node in patients with papillary thyroid carcinoma. Eur J Surg Oncol. 2007;33(9):1075–80.
Pellizo M, Rubello D, Boschin I, Piotto A, Paggetta C, Toniato A, et al. Contribution of SLN investigation with 99mTc-nanocolloid in clinical staging of thyroid cancer: technical feasibility. Eur J Nucl Med Mol Imaging. 2007;34(6):934–8.
Wang J, Deng X, Jin X, Zhang C, Zhou J, Zhou Q, et al. Surgical exploration of the sentinel lymph nodes in the papillary thyroid carcinoma. Rev Laryngol Otol Rhinol (Bord). 2008;129(4-5):285–7.
Boschin I, Toniato A, Piotto A, Ide E, Casara D, Guolo A, et al. 99Tc nanocolloid sentinel node procedure in thyroid carcinoma. Langenbecks Arch Surg. 2008;393(5):705–8.
Takeyama H, Tabei I, Uchida K, Morikawa T. Sentinel node biopsy for follicular tumours of the thyroid gland. Br J Surg. 2009;96(5):490–5.
Lee S, Choi J, Lim H, Kim W, Choe J, Lee J, et al. Sentinel lymph node biopsy in papillary thyroid cancer: comparison study of blue dye method and combined radioisotope and blue dye method in papillary thyroid cancer. Eur J Surg Oncol. 2009;35(9):974–9.
Zhang B, Yan D, Liu L, Niu L, An C, Zhang Z, et al. Sentinel lymph node biopsy in papillary thyroid cancer. Zhonghua Zhong Liu Za Zhi. 2010;32(10):782–5.
Cunningham D, Yao K, Turner R, Singer F, Van Herle A, Giuliano A. Sentinel lymph node biopsy for papillary thyroid cancer: 12 years of experience at a single institution. Ann Surg Oncol. 2010;17(11):2070–5.
Sabaté-Fernández M, Roca I, Kisiel N, Garcia-Burillo A, Porta F, Gonzalez O, et al. Usefulness of selective sentinel lymph node biopsy in the diagnosis of extension of papillary thyroid cancer. Annual Congress of the EANM 2011. October 2011, Birmingham. Eur J Nucl Med Mol Imaging. 2011;38 Suppl 2:OP305.
Amir A, Payne R, Richardson K, Hier M, Mlynarek A, Caglar D. Sentinel lymph node biopsy in thyroid cancer: it can work but there are pitfalls. Otolaryngol Head Neck Surg. 2011;145(5):723–6.
Huang O, Wo W, Wang O, You J, Huang D, Hu X, et al. Sentinel lymph node biopsy is unsuitable for routine practice in younger female patients with unilateral low-risk papillary thyroid carcinoma. BMC Cancer. 2011;11:386.
Hao R, Chen J, Zhao L, Liu C, Wang O, Huang G, et al. Sentinel lymph node biopsy using carbon nanoparticles for Chinese patients with papillary thyroid microcarcinomas. Eur J Surg Oncol. 2012;38(8):718–24.
Li X, Ma H, Tian X, Jin X. Elective neck dissection in papillary thyroid carcinoma patients. Acta Chir Belg. 2012;112(1):44–50.
Ji Y, Lee K, Park Y, Hong S, Paik S, Tae K. Clinical efficacy of sentinel lymph node biopsy using methylene blue dye in clinically node-negative papillary thyroid carcinoma. Ann Surg Oncol. 2012;19(6):1868–73.
Rajmakers PG, Paul MA, Lips P. Sentinel node detection in patients with thyroid carcinoma: a meta-analysis. Word J Surg. 2008;32:1961–7.
Balasubramanian S, Harrison B. Systematic review and meta-analysis of sentinel node biopsy in thyroid cancer. Br J Surg. 2011;98(3):334–44.
Kaczka K, Celnik A, Luks B, Jasion J, Pomorski L. Sentinel lymph node biopsy techniques in thyroid pathologies – a meta-analysis. Endokrynol Pol. 2012;63(3):222–31.
Blumencranz P, Pieretti M, Allen K, Blumencranz L. Molecular analysis of breast sentinel lymph nodes. Surg Oncol Clin N Am. 2011;20:467–85.
Cserni G. Intraoperative analysis of sentinel lymph nodes in breast cancer by one-step nucleic acid amplification. J Clin Pathol. 2012;65:193–9.
Mijovic T, Richardson K, Payne RJ, How J. Sentinel lymph node biopsy in well differentiated thyroid cancer. In: Fahey T, editor. Updates in the understanding and management of thyroid cancer. Rijeka: InTech; 2012. p. 217–234.
Pelizzo M, Toniato A, Sorgato N, Losi A, Torresan F, Merante BI. 99Tc nanocolloid sentinel node procedure in papillary thyroid carcinoma: our mono-institutional experience on a large series of patients. Acta Otorhinolaryngol Ital. 2009;29:321–5.
Roh J, Park C. Sentinel lymph node biopsy as guidance for central neck dissection in patients with papillary thyroid carcinoma. Cancer. 2008;113:1527–31.
Lee S, Kim S, Hur S, Choe J, Kim J, Kim J. The efficacy of lateral neck sentinel lymph node biopsy in papillary thyroid carcinoma. World J Surg. 2011;35:2675–82.
Acknowledgments
This work was supported by grant FIS PI09/90440 from the Health Research Fund of the Spanish “Instituto de Salud Carlos III”.
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Garcia-Burillo, A., Roca Bielsa, I., Gonzalez, O. et al. SPECT/CT sentinel lymph node identification in papillary thyroid cancer: lymphatic staging and surgical management improvement. Eur J Nucl Med Mol Imaging 40, 1645–1655 (2013). https://doi.org/10.1007/s00259-013-2476-x
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DOI: https://doi.org/10.1007/s00259-013-2476-x