Annals of Surgical Oncology

, Volume 22, Supplement 3, pp 669–675 | Cite as

Feasibility of Charcoal Tattooing for Localization of Metastatic Lymph Nodes in Robotic Selective Neck Dissection for Papillary Thyroid Carcinoma

  • Chang Myeon Song
  • Jeong Seon Park
  • Woosung Park
  • Yong Bae Ji
  • Seok Hyun Cho
  • Kyung TaeEmail author
Endocrine Tumors



This study aimed to evaluate the feasibility and effectiveness of ultrasound-guided charcoal tattooing in locating metastatic lymph nodes in robotic selective neck dissection (SND) for papillary thyroid carcinoma (PTC).


The overall study group comprised 21 patients with PTC who underwent robotic SND via a unilateral transaxillary approach for treatment of suspicious lymph node metastasis in the lateral compartment. Charcoal suspension was injected into 10 of the patients (total of 23 lesions) 1 day before robotic SND. The authors evaluated the location of the tattoos, the success rate of localization, the intraoperative detection rate, and the complications associated with the procedure. The perioperative results were compared with those in the control group of 11 patients who did not receive charcoal tattooing.


Charcoal suspension was successfully injected into 22 of the 23 suspicious lymph nodes (95.7 %). The remaining lesion was located posterior to the internal jugular vein. Therefore, the charcoal was injected into the soft tissue around the lymph node. Ultrasound-guided injections were well tolerated in all the patients, and no major complications occurred. All the charcoal-tattooed lesions were identified intraoperatively by the surgeon. The number of harvested and metastatic lymph nodes in the lateral compartment was greater in the patients with charcoal tattoo localization than in the control group. The two groups did not differ in terms of perioperative complications, operation time, or volume of drainage.


Ultrasound-guided charcoal tattooing for localization of metastatic lymph nodes is feasible and effective in robotic SND for the treatment of PTC with lateral compartment lymph node metastasis.


Charcoal Papillary Thyroid Carcinoma Neck Dissection Lateral Compartment Suspicious Lymph Node 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Conflict of interest

There are no conflicts of interest.


  1. 1.
    Schneider DF, Chen H, Sippel RS. Impact of lymph node ratio on survival in papillary thyroid cancer. Ann Surg Oncol. 2013;20:1906–11.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Zaydfudim V, Feurer ID, Griffin MR, Phay JE. The impact of lymph node involvement on survival in patients with papillary and follicular thyroid carcinoma. Surgery. 2008;144:1070–7.PubMedCrossRefGoogle Scholar
  3. 3.
    Ito Y, Kudo T, Takamura Y, Kobayashi K, Miya A, Miyauchi A. Lymph node recurrence in patients with N1b papillary thyroid carcinoma who underwent unilateral therapeutic modified radical neck dissection. World J Surg. 2012;36:593–7.PubMedCrossRefGoogle Scholar
  4. 4.
    Tae K, Ji YB, Song CM, Min HJ, Lee SH, Kim DS. Robotic lateral neck dissection by a gasless unilateral axillobreast approach for differentiated thyroid carcinoma: our early experience. Surg Laparosc Endosc Percutan Tech. 2014;24:128–32.CrossRefGoogle Scholar
  5. 5.
    Tae K, Ji YB, Jeong JH, Lee SH, Jeong MA, Park CW. Robotic thyroidectomy by a gasless unilateral axillo-breast or axillary approach: our early experiences. Surg Endosc. 2011;25:221–8.PubMedCrossRefGoogle Scholar
  6. 6.
    Tae K, Ji YB, Cho SH, Lee SH, Kim DS, Kim TW. Early surgical outcomes of robotic thyroidectomy by a gasless unilateral axillo-breast or axillary approach for papillary thyroid carcinoma: 2 years’ experience. Head Neck. 2012;34:617–25.PubMedCrossRefGoogle Scholar
  7. 7.
    Song CM, Cho YH, Ji YB, Jeong JH, Kim DS, Tae K. Comparison of a gasless unilateral axillo-breast and axillary approach in robotic thyroidectomy. Surg Endosc. 2013;27:3769–75.PubMedCrossRefGoogle Scholar
  8. 8.
    Lannin DR, Grube B, Black DS, Ponn T. Breast tattoos for planning surgery following neoadjuvant chemotherapy. Am J Surg. 2007;194:518–20.PubMedCrossRefGoogle Scholar
  9. 9.
    Canavese G, Catturich A, Vecchio C, Tomei D, Estienne M, Moresco L, et al. Preoperative localization of nonpalpable lesions in breast cancer by charcoal suspension. Eur J Surg Oncol. 1995;21:47–9.PubMedCrossRefGoogle Scholar
  10. 10.
    Naveau S, Bonhomme L, Preaux N, Chaput JC. A pure charcoal suspension for colonoscopic tattoo. Gastrointest Endosc. 1991;37:624–5.PubMedCrossRefGoogle Scholar
  11. 11.
    Lee DW, Ji YB, Sung ES, Park JS, Lee YJ, Park DW, et al. Roles of ultrasonography and computed tomography in the surgical management of cervical lymph node metastases in papillary thyroid carcinoma. Eur J Surg Oncol. 2013;39:191–6.PubMedCrossRefGoogle Scholar
  12. 12.
    Song CM, Lee DW, Ji YB, Jeong JH, Park JH, Tae K. Frequency and pattern of central lymph node metastasis in papillary carcinoma of the thyroid isthmus. Head Neck. doi: 10.1002/hed.24009. [Online 12 January 2015].
  13. 13.
    Lesnik D, Cunnane ME, Zurakowski D, Acar GO, Ecevit C, Mace A, et al. Papillary thyroid carcinoma nodal surgery directed by a preoperative radiographic map utilizing CT scan and ultrasound in all primary and reoperative patients. Head Neck. 2014;36:191–202.PubMedCrossRefGoogle Scholar
  14. 14.
    Binyousef HM, Alzahrani AS, Al-Sobhi SS, Al SH, Chaudhari MA, Raef HM. Preoperative neck ultrasonographic mapping for persistent/recurrent papillary thyroid cancer. World J Surg. 2004;28:1110–14.PubMedCrossRefGoogle Scholar
  15. 15.
    Wu LM, Gu HY, Qu XH, Zheng J, Zhang W, Yin Y, et al. The accuracy of ultrasonography in the preoperative diagnosis of cervical lymph node metastasis in patients with papillary thyroid carcinoma: a meta-analysis. Eur J Radiol. 2012;81:1798–805.PubMedCrossRefGoogle Scholar
  16. 16.
    Xiang D, Hong Y, Zhang B, Huang P, Li G, Wang P, Li Z, et al. Contrast-enhanced ultrasound (CEUS) facilitated US in detecting lateral neck lymph node metastasis of thyroid cancer patients: diagnosis value and enhancement patterns of malignant lymph nodes. Eur Radiol. 2014;24:2513–9.PubMedCrossRefGoogle Scholar
  17. 17.
    Na DK, Choi YJ, Choi SH, Kook SH, Park HJ. Evaluation of cervical lymph node metastasis in thyroid cancer patients using real-time CT-navigated ultrasonography: preliminary study. Ultrasonography. 2015;34:39–44.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Desai D, Jeffrey RB, McDougall IR, Weigel RJ. Intraoperative ultrasonography for localization of recurrent thyroid cancer. Surgery. 2001;129:498–500.PubMedGoogle Scholar
  19. 19.
    Negele T, Meisetschlager G, Bruckner T, Scheidhauer K, Schwaiger M, Vogelsang H. Radio-guided surgery for persistent differentiated papillary thyroid cancer: case presentations and review of the literature. Langenbecks Arch Surg. 2006;391:178–86.PubMedCrossRefGoogle Scholar
  20. 20.
    Travagli JP, Cailleux AF, Ricard M, Baudin E, Caillou B, Parmentier C, et al. Combination of radioiodine (131I) and probe-guided surgery for persistent or recurrent thyroid carcinoma. J Clin Endocrinol Metab. 1998;83:2675–80.PubMedCrossRefGoogle Scholar
  21. 21.
    Kim WW, Kim JS, Hur SM, Kim SH, Lee SK, Choi JH, et al. Radioguided surgery using an intraoperative PET probe for tumor localization and verification of complete resection in differentiated thyroid cancer: a pilot study. Surgery. 2011;149:416–24.PubMedCrossRefGoogle Scholar
  22. 22.
    Rubello D, Salvatori M, Casara D, Piotto A, Toniato A, Gross MD, et al. 99mTc-sestamibi radio-guided surgery of loco-regional 131Iodine-negative recurrent thyroid cancer. Eur J Surg Oncol. 2007;33:902–6.PubMedCrossRefGoogle Scholar
  23. 23.
    Seifi A, Axelrod H, Nascimento T, Salam Z, Karimi S, Avestimehr S, et al. Migration of guidewire after surgical breast biopsy: an unusual case report. Cardiovasc Intervent Radiol. 2009;32:1087–90PubMedCrossRefGoogle Scholar
  24. 24.
    Martinez SR, Gelfand M, Hourani HS, Sorrento JJ, Mohan EP. Cardiac injury during needle localized surgical breast biopsy. J Surg Oncol. 2003;82:261–5.PubMedCrossRefGoogle Scholar
  25. 25.
    Triponez F, Poder L, Zarnegar R, Goldstein R, Roayaie K, Feldstein V, et al. Hook needle-guided excision of recurrent differentiated thyroid cancer in previously operated neck compartments: a safe technique for small, nonpalpable recurrent disease. J Clin Endocrinol Metab. 2006;91:4943–7.PubMedCrossRefGoogle Scholar
  26. 26.
    Duprez R, Lebas P, Marc OS, Mongeois E, Emy P, Michenet P. Preoperative US-guided hook-needle insertion in recurrent lymph nodes of papillary thyroid cancer: a help for the surgeon. Eur J Radiol. 2010;73:40–2.PubMedCrossRefGoogle Scholar
  27. 27.
    Ryan WR, Orloff LA. Intraoperative tumor localization with surgeon-performed ultrasound-guided needle dye injection. Laryngoscope. 2011;121:1651–5.PubMedCrossRefGoogle Scholar
  28. 28.
    Lee JH, Chang CH, Park CH, Kim JK. Methylene blue dye-induced skin necrosis in immediate breast reconstruction: evaluation and management. Arch Plast Surg. 2014;41:258–63.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Mathieu MC, Bonhomme-Faivre L, Rouzier R, Seiller M, Barreau-Pouhaer L, Travagli JP. Tattooing breast cancers treated with neoadjuvant chemotherapy. Ann Surg Oncol. 2007;14:2233–8.PubMedCrossRefGoogle Scholar
  30. 30.
    Svane G. A stereotaxic technique for preoperative marking of nonpalpable breast lesions. Acta Radiol Diagn Stockh. 1983;24:145–51.PubMedCrossRefGoogle Scholar
  31. 31.
    Ko K, Han BK, Jang KM, Choe YH, Shin JH, Yang JH, et al. The value of ultrasound-guided tattooing localization of nonpalpable breast lesions. Korean J Radiol. 2007;8:295–301.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Hartl DM, Chami L, Al Ghuzlan A, Leboulleux S, Baudin E, Schlumberger M, et al. Charcoal suspension tattoo localization for differentiated thyroid cancer recurrence. Ann Surg Oncol. 2009;16:2602–8.PubMedCrossRefGoogle Scholar
  33. 33.
    Kang TW, Shin JH, Han BK, Ko EY, Kang SS, Hahn SY, et al. Preoperative ultrasound-guided tattooing localization of recurrences after thyroidectomy: safety and effectiveness. Ann Surg Oncol. 2009;16:1655–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Soprani F, Bondi F, Puccetti M, Armaroli V. Charcoal tattoo localization for differentiated thyroid cancer recurrence in the central compartment of the neck. Acta Otorhinolaryngol Ital. 2012;32:87–92.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Chami L, Hartl D, Leboulleux S, Baudin E, Lumbroso J, Schlumberger M, et al. Preoperative localization of neck recurrences from thyroid cancer: charcoal tattooing under ultrasound guidance. Thyroid. 2015;25:341–6.PubMedCrossRefGoogle Scholar
  36. 36.
    Kwon H, Tae SY, Kim SJ, Jung KC, Kim JH, Lee KE, et al. Role of charcoal tattooing in localization of recurred papillary thyroid carcinoma: initial experiences. Ann Surg Treat Res. 2015;88:140–4.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Bonhomme-Faivre L, Depraetere P, Savelli MP, Amdidouche D, Bizi E, Seiller M, et al. Charcoal suspension for tumor labelling modifies macrophage activity in mice. Life Sci. 2000;66:817–27.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2015

Authors and Affiliations

  • Chang Myeon Song
    • 1
  • Jeong Seon Park
    • 2
  • Woosung Park
    • 1
  • Yong Bae Ji
    • 1
  • Seok Hyun Cho
    • 1
  • Kyung Tae
    • 1
    Email author
  1. 1.Department of Otolaryngology-Head and Neck Surgery, College of MedicineHanyang UniversitySeoulKorea
  2. 2.Department of Radiology, College of MedicineHanyang UniversitySeoulKorea

Personalised recommendations