Indocyanine green fluorescence angiography in transoral endoscopic thyroidectomy for papillary thyroid cancer

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OBJECTIVE

To evaluate the effectiveness of ICG angiography in patients with papillary thyroid cancer (PTC) undergoing transoral endoscopic thyroidectomy (TOETVA) and selective neck dissection (level VI).

MATERIAL AND METHODS

A retrospective analysis included 20 patients with PTC who underwent TOETVA with selective neck dissection (level VI) between September and December 2022. ICG was administered intravenously (5 mg ´ 3 times). We analyzed parathyroid glands by visual examination and ICG angiography. Fluorescence of all glands was assessed.

RESULTS

Twenty patients underwent ICG angiography during TOETVA. A total of 68 parathyroid glands were identified. Only 76.5% (52/68) of parathyroid glands were identified at initial visual examination. ICG angiography additionally localized 12 glands that improved detection to 94.1% (64/68). At least one well-vascularized parathyroid gland was demonstrated by ICG angiography in 16 patients. In all these patients, serum parathyroid hormone was normal in 1 and 10 days after surgery. Two out of four patients who failed to identify a well-vascularized parathyroid gland developed transient hypoparathyroidism. There were no intraoperative and postoperative complications associated with ICG angiography.

CONCLUSION

ICG angiography was simple, safe and effective for better identification and preservation of parathyroid glands in patients with PTC undergoing TOETVA. This method was valuable for assessing the viability and function of parathyroid glands and predicting postoperative hypocalcemia.

Keywords:

fluorescence

hypoparathyroidism

indocyanin green angiography

parathyroid gland

thyroid surgery

papillary thyroid cancer

Authors:

Polkin V.V.

Tsyb Medical Radiology Research Center

ORCID: 0000-0003-0857-321X

Isaev P.A.

Tsyb Medical Radiology Research Center

ORCID: 0000-0001-9831-4814

Plugar A.K.

Tsyb Medical Radiology Research Center

ORCID: 0000-0002-0049-4309

Ilyin A.A.

Tsyb Medical Radiology Research Center

ORCID: 0000-0002-6581-633X

Ivanov S.A.

Tsyb Medical Radiology Research Center;
People’s Friendship University of Russia

ORCID: 0000-0001-7689-6032

Kaprin A.D.

National Medical Research Radiology Center;
People’s Friendship University of Russia;
Herzen Moscow Oncology Research Institute

SPIN RSCI: 1759-8101
Scopus AuthorID: 6602709853
ResearcherID: K-1445-2014
ORCID: 0000-0001-8784-8415

Received:

06.06.2023

Accepted:

28.06.2023

List of references:

Revishvili A.SH. Hirurgicheskaya pomoshch’ v Rossijskoj Federacii. M. 2022. (In Russ.).
Kaprin AD, Starinskij VV, Shahzadova AO. Zlokachestvennye novoobrazovaniya v Rossii v 2021 godu (zabolevaemost’ i smertnost’). M.: MNIOI im. P.A. Gercena — filial FGBU «NMIC radiologii» Minzdrava Rossii; 2022. (In Russ.).
Kim J, Gosnell JE, Roman SA. Geographic influences in the global rise of thyroid cancer. Nature Reviews. Endocrinology. 2020;16(1):17-29. https://doi.org/10.1038/s41574-019-0263-x
Puxeddu E, Tallini G, Vanni R. What Is New in Thyroid Cancer: The Special Issue of the Journal Cancers. Cancers. 2020;12(10):3036. https://doi.org/10.3390/cancers12103036
Edafe O, Antakia R, Laskar N, Uttley L, Balasubramanian SP. Systematic review and meta-analysis of predictors of post-thyroidectomy hypocalcaemia. British Journal of Surgery. 2014;101(4):307-320. https://doi.org/10.1002/bjs.9384
Papaleontiou M, Hughes DT, Guo C, Banerjee M, Haymart MR. Population-Based Assessment of Complications Following Surgery for Thyroid Cancer. The Journal of Clinical Endocrinology and Metabolism. 2017;102(7):2543-2551. https://doi.org/10.1210/jc.2017-00255
Teshima M, Otsuki N, Morita N, Furukawa T, Shinomiya H, Shinomiya H, Nibu KI. Postoperative hypoparathyroidism after total thyroidectomy for thyroid cancer. Auris, Nasus, Larynx. 2018;45(6):1233-1238. https://doi.org/10.1016/j.anl.2018.04.008
Vasileiadis I, Karatzas T, Charitoudis G, Karakostas E, Tseleni-Balafouta S, Kouraklis G. Association of Intraoperative Neuromonitoring With Reduced Recurrent Laryngeal Nerve Injury in Patients Undergoing Total Thyroidectomy. JAMA Otolaryngology — Head and Neck Surgery. 2016;142(10):994-1001. https://doi.org/10.1001/jamaoto.2016.1954
Orloff LA, Wiseman SM, Bernet VJ, Fahey TJ 3rd, Shaha AR, Shindo ML, Snyder SK, Stack BC Jr, Sunwoo JB, Wang MB. American Thyroid Association Statement on Postoperative Hypoparathyroidism: Diagnosis, Prevention, and Management in Adults. Thyroid. 2018;28(7):830-841. https://doi.org/10.1089/thy.2017.0309
Binder-Foucard F, Bossard N, Delafosse P, Belot A, Woronoff AS, Remontet L, French Network of Cancer Registries (Francim). Cancer incidence and mortality in France over the 1980-2012 period: solid tumors. Revue d’Epidemiologie et de Sante Publique. 2014;62:95-108. https://doi.org/10.1016/j.respe.2013.11.073
De Leeuw F, Breuskin I, Abbaci M, Casiraghi O, Mirghani H, Ben Lakhdar A, et al. Intraoperative near-infrared imaging for parathyroid gland identification by auto-fluorescence: a feasibility study. World Journal of Surgery. 2016;40(9):2131-2138. https://doi.org/10.1007/s00268-016-3571-5
Lorente-Poch L, Sancho JJ, Ruiz S, Sitges-Serra A. Importance of in situ preservation of parathyroid glands during total thyroidectomy. British Journal of Surgery. 2015;102(4):359-367. https://doi.org/10.1002/bjs.9676
Lorente-Poch L, Sancho JJ, Muñoz-Nova JL, Sánchez-Velázquez P, Sitges-Serra A. Defining the syndromes of parathyroid failure after total thyroidectomy. Gland Surgery. 2015;4(1):82-90. https://doi.org/10.3978/j.issn.2227-684X.2014.12.04
Mittendorf E, McHenry C. Complications and sequelae of thyroidectomy and an analysis of surgeon experience and outcome. Surgical Technology International. 2004;12:152-157.
Sapalidis K, Papanastasiou A, Fyntanidou V, Aidoni Z, Michalopoulos N, Katsaounis A, Amaniti A, Zarogoulidis P, Koulouris C, Giannakidis D, Ioannidis A, Katsios IN, Romanidis K, Oikonomou P, Kesisoglou I, Kosmidis C. Comparison between magnification techniques and direct vision in thyroid surgery: a systematic review and meta-analysis. Medicina. 2019;55(11):725. https://doi.org/10.3390/medicina55110725
André N, Pascual C, Baert M, Biet-Hornstein A, Page C. Impact of incidental parathyroidectomy and mediastinal-recurrent cellular and lymph-node dissection on parathyroid function after total thyroidectomy. European Annals of Otorhinolaryngology, Head and Neck Diseases. 2020;137(2):107-110. https://doi.org/10.1016/j.anorl.2020.01.001
Chang YK, Lang BHH. To identify or not to identify parathyroid glands during total thyroidectomy. Gland Surgery. 2017;6(suppl 1):20-29. https://doi.org/10.21037/gs.2017.06.13
Dudley NE. Methylene blue for rapid identification of the parathyroids. British Medical Journal. 1971;3(5776):680-681. https://doi.org/10.1136/bmj.3.5776.680
Han N, Bumpous J, Goldstein R, Fleming M, Flynn M. Intra-operative parathyroid identification using methylene blue in parathyroid surgery. The American Surgeon. 2007;73(8):820-823. https://doi.org/10.1177/000313480707300819
Patel HP, Chadwick DR, Harrison BJ, Balasubramanian SP. Systematic review of intravenous methylene blue in parathyroid surgery. British Journal of Surgery. 2012;99(10):1345-1351. https://doi.org/10.1002/bjs.8814
Prosst RL, Schroeter L, Gahlen J. Enhanced ALA-induced fluorescence in hyperparathyroidism. Journal of Photochemistry and Photobiology. B, Biology. 2005;79(1):79-82. https://doi.org/10.1016/j.jphotobiol.2004.11.019
Prosst R, Weiß J, Hupp L, Willeke F, Post S. Fluorescence-guided minimally invasive parathyroidectomy: clinical experience with a novel intraoperative detection technique for parathyroid glands. World Journal of Surgery. 2010;34(9):2217-2222. https://doi.org/10.1007/s00268-010-0621-2
Paras C, Keller M, Mahadevan-Jansen A, White L, Phay J. Near-infrared autofluorescence for the detection of parathyroid glands. Journal of Biomedical Optics. 2011;16(6):1-5. https://doi.org/10.1117/1.3583571
McWade MA, Sanders ME, Broome JT, Solórzano CC, Mahadevan-Jansen A. Establishing the clinical utility of autofluorescence spectroscopy for parathyroid detection. Surgery. 2016;159(1):193-203. https://doi.org/10.1016/j.surg.2015.06.047
Falco J, Dip F, Quadri P, Fuente M, Rosenthal R. Cutting edge in thyroid surgery: autofluorescence of parathyroid glands. Journal of the American College of Surgeons. 2016;223(2):374-380. https://doi.org/10.1016/j.jamcollsurg.2016.04.049
Solórzano CC, Thomas G, Berber E, Wang TS, Randolph GW, Duh QY, Triponez F. Current state of intraoperative use of near infrared fluorescence for parathyroid identification and preservation. Surgery. 2021;169(4):868-878. https://doi.org/10.1016/j.surg.2020.09.014
Spartalis E, Ntokos G, Georgiou K, Zografos G, Tsourouflis G, Dimitroulis D, Nikiteas NI. Intraoperative Indocyanine Green (ICG) Angiography for the Identification of the Parathyroid Glands: Current Evidence and Future Perspectives. In Vivo. 2020;34(1):23-32. https://doi.org/10.21873/invivo.11741
DeLong JC, Ward EP, Lwin TM, Brumund KT, Kelly KJ, Horgan S, Bouvet M. Indocyanine green fluorescence-guided parathyroidectomy for primary hyperparathyroidism. Surgery. 2018;163(2):388-392. https://doi.org/10.1016/j.surg.2017.08.018
Zaidi N, Bucak E, Yazici P, Soundararajan S, Okoh A, Yigitbas H, Dural C, Berber E. The feasibility of indocyanine green fluorescence imaging for identifying and assessing the perfusion of parathyroid glands during total thyroidectomy. Journal of Surgical Oncology. 2016;113(7):775-778. https://doi.org/10.1002/jso.24237
Anuwong A, Ketwong K, Jitpratoom P, Sasanakietkul T, Duh QY. Safety and Outcomes of the Transoral Endoscopic Thyroidectomy Vestibular Approach. JAMA Surgery. 2018;153(1):21-27. https://doi.org/10.1001/jamasurg.2017.3366
Xing Z, Qiu Y, Abuduwaili M, Xia B, Fei Y, Zhu J, Su A. Surgical outcomes of different approaches in robotic assisted thyroidectomy for thyroid cancer: A systematic review and Bayesian network meta-analysis International Journal of Surgery. 2021;89:105941. https://doi.org/10.1016/j.ijsu.2021.105941
Kandil E, Hammad AY, Walvekar RR, Hu T, Masoodi H, Mohamed SE, Deniwar A, Stack BC, Jr. Robotic Thyroidectomy Versus Nonrobotic Approaches: A Meta-Analysis Examining Surgical Outcomes. Surgical Innovation. 2016;23(3):317-325. https://doi.org/10.1177/1553350615613451
Wu YJ, Cheng BC, Chiu CH, Huang SC, Li LC, Chung SY, Den Chen K, Pan CC, Li JY, Lin HW, Chen YH, Liang PL, Co JS, Chi SY, Chou FF, Lin CC. Successful Modified Transoral Endoscopic Parathyroidectomy Vestibular Approach For Secondary Hyperparathyroidism with Ectopic Mediastinal Glands. Surgical Laparoscopy, Endoscopy and Percutaneous Techniques. 2019;29(6):88-93. https://doi.org/10.1097/SLE.0000000000000727
Cohen O, Tufano RP, Anuwong A, Shaha AR, Olsen KD, Zafereo M, Rinaldo A, Mäkitie AA, Nixon IJ, Russell JO, Ferlito A, Khafif A. Transoral endoscopic vestibular approach for thyroidectomy and parathyroidectomy — From promise to practice. American Journal of Otolaryngology. 2021;42(5):103022. https://doi.org/10.1016/j.amjoto.2021.103022
Yu HW, Chung JW, Yi JW, Song RY, Lee JH, Kwon H, Kim SJ, Chai YJ, Choi JY, Lee KE. Intraoperative localization of the parathyroid glands with indocyanine green and Firefly(R) technology during BABA robotic thyroidectomy. Surgical Endoscopy. 2017;31(7):3020-3027. https://doi.org/10.1007/s00464-016-5330-y
Turan MI, Celik M, Erturk MS. Indocyanine green fluorescence angiography-guided transoral endoscopic thyroidectomy and parathyroidectomy: First clinical report. Photodiagnosis and Photodynamic Therapy. 2020;32:102028. https://doi.org/10.1016/j.pdpdt.2020.102028
Zhang X, Li JG, Zhang SZ, Chen G. Comparison of indocyanine green and carbon nanoparticles in endoscopic techniques for central lymph nodes dissection in patients with papillary thyroid cancer. Surgical Endoscopy. 2020;34(12):5354-5359. https://doi.org/10.1007/s00464-019-07326-4
Pol’kin VV, Isaev PA, Il’in AA, Plugar’ AK, Kaprin AD, Ivanov SA. Sposob endoskopicheskogo udaleniya shchitovidnoj zhelezy pri zlokachestvennyh novoobrazovaniyah. Zayavka na izobretenie №2022123645, opublikovano 24.10.22, byull. 30. (In Russ.).
Barrios L, Shafqat I, Alam U, Ali N, Patio C, Filarski CF, Bankston H, Mallen-St Clair J, Luu M, Zumsteg ZS, Adashek K, Chen Y, Jain M, Braunstein GD, Sacks WL, Ho AS. Incidental parathyroidectomy in thyroidectomy and central neck dissection. Surgery. 2021;169(5):1145-1151. https://doi.org/10.1016/j.surg.2020.11.023
Sakorafas GH, Stafyla V, Bramis C, Kotsifopoulos N, Kolettis T, Kassaras G. Incidental parathyroidectomy during thyroid surgery: An underappreciated complication of thyroidectomy. World Journal of Surgery. 2005;29(12):1539-1543. https://doi.org/10.1007/s00268-005-0032-y
Vidal Fortuny J, Belfontali V, Sadowski SM, Karenovics W, Guigard S, Triponez F. Parathyroid gland angiography with indocyanine green fluorescence to predict parathyroid function after thyroid surgery. British Journal of Surgery. 2016;103(5):537-543. https://doi.org/10.1002/bjs.10101
Rudin AV, McKenzie TJ, Thompson GB, Farley DR, Lyden ML. Evaluation of Parathyroid Glands with Indocyanine Green Fluorescence Angiography after Thyroidectomy. World Journal of Surgery. 2019;43(6):1538-1543. https://doi.org/10.1007/s00268-019-04909-z

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