Abstract
Background
Recurrent laryngeal nerve (RLN) injury after thyroidectomy is relatively common. Locating the RLN prior to thyroid dissection is paramount to avoid injury. We developed a fluorescence imaging system that permits nerve autofluorescence. We aimed to determine the sensitivity and specificity of fluorescence imaging at detecting the RLN relative to thyroid and other background tissue and compared it to white light.
Methods
In this prospective study, 65 patients underwent thyroidectomy from January to April 2022 (16 bilateral thyroid resections) using white and fluorescent light. Fluorescence intensity [relative fluorescence units (RFU)] was recorded for RLN, thyroid, and background. RFU mean, minimum, and maximum values were calculated using Image J software. Thirty randomly selected pairs of white and fluorescent light images were independently reviewed by two examiners to compare RLN detection rate, number of branches, and length and minimum width of nerves visualized. Parametric and nonparametric statistical analysis was performed.
Results
All 81 RNLs observed were visualized more clearly under fluorescence (mean intensity, µ = 134.3 RFU) than either thyroid (µ = 33.7, p < 0.001) or background (µ = 14.4, p < 0.001). Forest plots revealed no overlap between RLN intensity and that of either other tissue. Sensitivity and specificity for RLN were 100%. All 30 RLNs and all 45 nerve branches were clearly visualized under fluorescence, versus 17 and 22, respectively, with white light (both p < 0.001). Visible nerve length was 2.5 × as great with fluorescence as with white light (µ = 1.90 vs. 0.76 cm, p < 0.001).
Conclusions
In 65 patients and 81 nerves, RLN detection was markedly and consistently enhanced with autofluorescence neuro-imaging during thyroidectomy, with 100% sensitivity and specificity.
Similar content being viewed by others
References
Gouma DJ, Go PM (1994) Bile duct injury during laparoscopic and conventional cholecystectomy. J Am Coll Surg 178(3):229–233
Ciaramitaro P, Mondelli M, Logullo F et al (2010) Traumatic peripheral nerve injuries: epidemiological findings, neuropathic pain and quality of life in 158 patients. J Peripher Nerv Syst 15(2):120–127
Kretschmer T, Antoniadis G, Braun V, Rath SA, Richter HP (2001) Evaluation of iatrogenic lesions in 722 surgically treated cases of peripheral nerve trauma. J Neurosurg 94(6):905–912
Zakaria HM, Al Awad NA, Al Kreedes AS et al (2011) Recurrent laryngeal nerve injury in thyroid surgery. Oman Med J 26(1):34–38
Bu Bshait M, Alyami H, Al-Osail E, Al AH (2018) Ipsilateral hypoglossal nerve palsy following left hemithyroidectomy: case report and review of literature. Int J Surg Case Rep 51:5–7
Miller MC, Spiegel JR (2008) Identification and monitoring of the recurrent laryngeal nerve during thyroidectomy. Surg Oncol Clin N Am 17(1):121–144, viii–ix
Sakorafas GH, Kokoropoulos P, Lappas C, Sampanis D, Smyrniotis V (2012) External branch of the superior laryngeal nerve: applied surgical anatomy and implications in thyroid surgery. Am Surg 78(9):986–991
Zábrodský M, Bouček J, Kastner J, Kuchař M, Chovanec M, Betka J (2012) Immediate revision in patients with bilateral recurrent laryngeal nerve palsy after thyroid and parathyroid surgery. How worthy is it? Acta Otorhinolaryngol Ital 32(4):222–228
Chrysikos D, Sgantzos M, Tsiaoussis J et al (2019) Non-recurrent right laryngeal nerve: a rare anatomic variation encountered during a total thyroidectomy. Acta Medica (Hradec Kralove) 62(2):69–71
Henry BM, Vikse J, Graves MJ et al (2017) Variable relationship of the recurrent laryngeal nerve to the inferior thyroid artery: a meta-analysis and surgical implications. Head Neck 39(1):177–186
Polednak AP (2017) Relationship of the recurrent laryngeal nerve to the inferior thyroid artery: a comparison of findings from two systematic reviews. Clin Anat (New York, NY) 30(3):318–321
Sheikh NA, Khattak SF, Aleem A, Nadeem K (2019) Diverse anatomical configuration of recurrent laryngeal nerve in relation to inferior thyroid artery, an experience with 51 thyroidectomies. J Ayub Med Coll Abbottabad 31(2):168–171
Wu G, Wang K (2017) A novel variation of the recurrent laryngeal nerve. BMC Surg 17(1):66
Casella C, Pata G, Nascimbeni R, Mittempergher F, Salerni B (2009) Does extralaryngeal branching have an impact on the rate of postoperative transient or permanent recurrent laryngeal nerve palsy? World J Surg 33(2):261–265
Sahli Z, Canner JK, Najjar O, Schneider EB, Prescott JD, Russell JO et al (2019) Association between age and patient-reported changes in voice and swallowing after thyroidectomy. Laryngoscope 129(2):519–524
Neri G, Castiello F, Vitullo F, De Rosa M, Ciammetti G, Croce A (2011) Post-thyroidectomy dysphonia in patients with bilateral resection of the superior laryngeal nerve: a comparative spectrographic study. Acta Otorhinolaryngol Ital 31(4):228–234
Liu X, Zhang D, Zhang G et al (2018) Laryngeal nerve morbidity in 1.273 central node dissections for thyroid cancer. Surg Oncol 27(2):21–25
Hoesli R, Brennan JR, Rosko AJ et al (2019) Intraoperative fluorescent angiography predicts Pharyngocutaneous fistula after salvage laryngectomy. Ann Surg Oncol 26(5):1320–1325
Abbaci M, De Leeuw F, Breuskin I et al (2018) Parathyroid gland management using optical technologies during thyroidectomy or parathyroidectomy: a systematic review. Oral Oncol 87:186–196
Dip F, Falco J, Verna S et al (2019) Randomized controlled trial comparing white light with near-infrared autofluorescence for parathyroid gland identification during total thyroidectomy. J Am Coll Surg 228(5):744–751
Dip F, Aleman R, Socolovsky M et al (2021) Nerve spectroscopy: understanding peripheral nerve autofluorescence through photodynamics. Surg Endosc 35(12):7104–7111
Dip F, Bregoli P, Falco J, White KP, Rosenthal RJ (2022) Nerve autofluorescence in near-ultraviolet light markedly enhances nerve visualization in vivo. Surg Endosc 36(3):1999–2005
Dip F, Rosenthal D, Socolovsky M et al (2022) Nerve autofluorescence under near-ultraviolet light: cutting-edge technology for intra-operative neural tissue visualization in 17 patients. Surg Endosc 36(6):4079–4089
Kennedy GT, McMillan MT, Sprys MH et al (2016) The influence of fellowship training on the practice of pancreatoduodenectomy. HPB (Oxford) 18(12):965–978
Koch M, Zenk J, Iro H (2010) Long-term results of morbidity after parotid gland surgery in benign disease. Laryngoscope 120(4):724–730
Dip FD, Roy M, Perrins S et al (2015) Technical description and feasibility of laparoscopic adrenal contouring using fluorescence imaging. Surg Endosc 29(3):569–574
Noureldine SI, Nazli Avci S, Isiktas G, Ergun O, Elshamy M, Berber E (2022) Detection of near-infrared autofluorescence from adrenal neoplasms: an initial experience. J Surg Oncol 126(2):257–262
Hingorani DV, Whitney MA, Friedman B et al (2018) Nerve-targeted probes for fluorescence-guided intraoperative imaging. Theranostics 8(15):4226–4437
de Veld DC, Skurichina M, Witjes MJ, Duin RP, Sterenborg HJ, Roodenburg JL (2005) Autofluorescence and diffuse reflectance spectroscopy for oral oncology. Lasers Surg Med 36(5):356–364
Oldfield EH (2012) Pituitary adenoma identification. J Neurosurg 116(5):933–934 (author reply 4)
Funding
None.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosures
Kevin White is an independent research consultant and statistician who was paid for his participation in this study. No other author received any funding for this study. Fernando Dip and Raul Rosenthal are on the Advisory Board for Axon Imaging Technologies. Fernando Dip is a company stakeholder. Dr. Falco has no potential conflicts of interest to declare.
Ethical approval
This study was conducted according to the Declaration of Helsinki as a statement of ethical principles for medical research involving human subjects, including research on identifiable human material and data. Prior to subject enrollment, Institutional Review Board (ethics) approval was received for this study from the Hospital de Clínicas Jose de San Martín where all patients underwent surgery. All patients signed informed patient/participant consent prior to enrollment.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dip, F., Falco, J., White, K. et al. Fluorescence imaging to visualize the recurrent laryngeal nerve during thyroidectomy procedures: analysis of 65 cases and 81 nerves. Surg Endosc 38, 1406–1413 (2024). https://doi.org/10.1007/s00464-023-10627-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-023-10627-4