Use of fluorescence image-guided surgery and autofluorescence in thyroid and parathyroid surgery

Abstract

Fluorescence-guided surgery (FGS) has seen increased interest in recent decades. Technological advances have made it more widely accessible for a variety of applications, including thyroid and parathyroid surgery. Parathyroid autofluorescence can be utilized to help identify parathyroid glands during thyroid or parathyroid surgery and reduce rates of postoperative hypocalcemia after thyroidectomy. Fluorescent dyes such as indocyanine green (ICG) may be used to evaluate perfusion of parathyroid glands during thyroid or parathyroid surgery and help guide decision-making about auto-transplantation or which gland to leave as a remnant. As an emerging technology, additional research is needed to determine the optimal use of FGS in thyroid and parathyroid surgery, including the developing field of molecularly targeted fluorophores. FGS is an exciting and promising field that may help make endocrine surgery safer, faster, and more effective.

Keywords

Indocyanine green / near-infrared fluorescence / fluorescence-guided surgery / autofluorescence / parathyroid / thyroid / endocrine surgery

References

[1] HAGUE EB.Fluorescing illumination in cataract surgery.Am J Ophthalmol1959;47:663-6

[2] Peck GC,Holbrook WA.Use of hematoporphyrin fluorescence in biliary and cancer surgery.Am Surg1955;21:181-8

[3] Sussman W.Detection of gynecologic cancer by fluorescence microscopy.Obstet Gynecol1959;13:273-7

[4] Homasson JP,Angebault M,Carnot F.Fluorescence as a guide to bronchial biopsy.Thorax1985;40:38-40 PMCID:PMC459975

[5] Leon MB,Bartorelli AL.Fluorescence-guided laser-assisted balloon angioplasty in patients with femoropopliteal occlusions.Circulation1990;81:143-55

[6] Mehlmann M,Stepp H.Fluorescence staining of laryngeal neoplasms after topical application of 5-aminolevulinic acid: preliminary results.Lasers Surg Med1999;25:414-20

[7] Silverman DG,Reilly CA.Fluorometric quantification of low-dose fluorescein delivery to predict amputation site healing.Surgery1987;101:335-41

[8] Girard N,Malhaire C.Innovative DIEP flap perfusion evaluation tool: qualitative and quantitative analysis of indocyanine green-based fluorescence angiography with the SPY-Q proprietary software.PLoS One2019;14:e0217698 PMCID:PMC6592538

[9] Reinhart MB,Blair LJ,Augenstein VA.Indocyanine green: historical context, current applications, and future considerations.Surg Innov2016;23:166-75

[10] Jafari MD,Halabi WJ.The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery.Surg Endosc2013;27:3003-8

[11] Griffiths M,Rozen WM.Indocyanine green-based fluorescent angiography in breast reconstruction.Gland Surg2016;5:133-49 PMCID:PMC4791345

[12] Solórzano CC,Berber E.Current state of intraoperative use of near infrared fluorescence for parathyroid identification and preservation.Surgery2021;169:868-78 PMCID:PMC7987670

[13] Agcaoglu O,Berber E.Indocyanine green fluorescence imaging for robotic adrenalectomy.Gland Surg2020;9:849-52 PMCID:PMC7347824

[14] Solórzano CC,Baregamian N.Detecting the near infrared autofluorescence of the human parathyroid: hype or opportunity?.Ann Surg2020;272:973-85

[15] van Manen L,Diana M.A practical guide for the use of indocyanine green and methylene blue in fluorescence-guided abdominal surgery.J Surg Oncol2018;118:283-300 PMCID:PMC6175214

[16] Paras C,White L,Mahadevan-Jansen A.Near-infrared autofluorescence for the detection of parathyroid glands.J Biomed Opt2011;16:067012

[17] WINKLER K.Determination of hepatic blood flow in man by cardio green.Scand J Clin Lab Invest1960;12:353-6

[18] Hope-Ross M,Gragoudas ES.Adverse reactions due to indocyanine green.Ophthalmology1994;101:529-33

[19] Alander JT,Laakso A.A review of indocyanine green fluorescent imaging in surgery.Int J Biomed Imaging2012;2012:940585 PMCID:PMC3346977

[20] Desmettre T,Mordon S.Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography.Surv Ophthalmol2000;45:15-27

[21] Dudley NE.Methylene blue for rapid identification of the parathyroids.Br Med J1971;3:680-1 PMCID:PMC1798947

[22] Khan MA,Chadwick DR.Prolonged postoperative altered mental status after methylene blue infusion during parathyroidectomy: a case report and review of the literature.Ann R Coll Surg Engl2007;89:W9-11 PMCID:PMC1964586

[23] Enny L,Singh KR,Garg S.Efficacy of fluorescein green dye in assessing intra-operative parathyroid gland vascularity and predicting post-thyroidectomy hypocalcaemia- a novel prospective cohort study.Indian J Endocrinol Metab2020;24:446-51 PMCID:PMC7810046

[24] Prosst RL,Hupp L,Post S.Fluorescence-guided minimally invasive parathyroidectomy: clinical experience with a novel intraoperative detection technique for parathyroid glands.World J Surg2010;34:2217-22

[25] Edafe O,Laskar N,Balasubramanian SP.Systematic review and meta-analysis of predictors of post-thyroidectomy hypocalcaemia.Br J Surg2014;101:307-20

[26] Rosato L,Bernante P.Complications of thyroid surgery: analysis of a multicentric study on 14,934 patients operated on in Italy over 5 years.World J Surg2004;28:271-6

[27] Pepe J,Biamonte F.Diagnosis and management of hypocalcemia.Endocrine2020;69:485-95

[28] Bove-Fenderson E.Hypocalcemic disorders.Best Pract Res Clin Endocrinol Metab2018;32:639-56

[29] Hujoel IA.The association between serum calcium levels and Chvostek sign: a population-based study.Neurol Clin Pract2016;6:321-8 PMCID:PMC5727700

[30] Falco J,Quadri P,Rosenthal R.Cutting edge in thyroid surgery: autofluorescence of parathyroid glands.J Am Coll Surg2016;223:374-80

[31] Dip F,Verna S.Randomized controlled trial comparing white light with near-infrared autofluorescence for parathyroid gland identification during total thyroidectomy.J Am Coll Surg2019;228:744-51

[32] Benmiloud F,Gras R.Association of autofluorescence-based detection of the parathyroid glands during total thyroidectomy with postoperative hypocalcemia risk: results of the PARAFLUO multicenter randomized clinical trial.JAMA Surg2020;155:106-12 PMCID:PMC6865247

[33] Yin S,Yang Z.Combined use of autofluorescence and indocyanine green fluorescence imaging in the identification and evaluation of parathyroid glands during total thyroidectomy: a randomized controlled trial.Front Endocrinol2022;13:897797 PMCID:PMC9243533

[34] Kim YS,Kahramangil B,Donmez M.The impact of near infrared fluorescence imaging on parathyroid function after total thyroidectomy.J Surg Oncol2020;122:973-9

[35] Marco AN, Palazzo FF. Near-infrared autofluorescence in thyroid and parathyroid surgery.Gland Surg2020;9:S136-46 PMCID:PMC7044090

[36] DiMarco A,Bloxham R,Tolley N.Does fluoroscopy prevent inadvertent parathyroidectomy in thyroid surgery?.Ann R Coll Surg Engl2019;101:508-13 PMCID:PMC6667958

[37] Lu W,Zhang P,Zhu J.Near-infrared autofluorescence imaging in thyroid surgery: a systematic review and meta-analysis.J Invest Surg2022;35:1723-32

[38] Wang B,Liu H,Wu J.The ability of near-infrared autofluorescence to protect parathyroid gland function during thyroid surgery: a meta-analysis.Front Endocrinol2021;12:714691 PMCID:PMC8573048

[39] 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.Br J Surg2016;103:537-43

[40] Jin H,He Z,Liao K.Application of a fluorescence imaging system with indocyanine green to protect the parathyroid gland intraoperatively and to predict postoperative parathyroidism.Adv Ther2018;35:2167-75

[41] Zaidi N,Yazici P.The feasibility of indocyanine green fluorescence imaging for identifying and assessing the perfusion of parathyroid glands during total thyroidectomy.J Surg Oncol2016;113:775-8

[42] Spartalis E,Georgiou K.Intraoperative indocyanine green (ICG) angiography for the identification of the parathyroid glands: current evidence and future perspectives.In Vivo2020;34:23-32 PMCID:PMC6984100

[43] Kim DH,Jung J,Hwang SH.Indocyanine green fluorescence for parathyroid gland identification and function prediction: systematic review and meta-analysis.Head Neck2022;44:783-91

[44] Vidal Fortuny J,Belfontali V.Randomized clinical trial of intraoperative parathyroid gland angiography with indocyanine green fluorescence predicting parathyroid function after thyroid surgery.Br J Surg2018;105:350-7 PMCID:PMC6084300

[45] Benmiloud F,Chiche L.Intraoperative mapping angiograms of the parathyroid glands using indocyanine green during thyroid surgery: results of the fluogreen study.World J Surg2022;46:416-24

[46] Rudin AV,Thompson GB,Lyden ML.Evaluation of parathyroid glands with indocyanine green fluorescence angiography after thyroidectomy.World J Surg2019;43:1538-43

[47] Razavi AC,Haddad A.Efficacy of indocyanine green fluorescence in predicting parathyroid vascularization during thyroid surgery.Head Neck2019;41:3276-81

[48] Hartl D OR,Breuskin I,Laplace-Builhé C. Intraoperative parathyroid gland identification using autofluorescence: pearls and pitfalls. Available from: https://www.surgeryresearchjournal.com/open-access/intraoperative-parathyroid-gland-identification-using-autofluorescence-pearls-and-pitfalls-6931.pdf [Last accessed on 29 Mar 2023]

[49] Shinden Y,Arima H.Intraoperative identification of the parathyroid gland with a fluorescence detection system.World J Surg2017;41:1506-12

[50] Demarchi MS,Lifante JC,Triponez F.Fluorescence image-guided surgery for thyroid cancer: utility for preventing hypoparathyroidism.Cancers2021;13:3792 PMCID:PMC8345196

[51] Matson J,Bouvet M.Rapid intraoperative perfusion assessment of parathyroid adenomas with ICG using a wide-field portable hand-held fluorescence imaging system.Am J Surg2022;223:686-93

[52] Barbieri D,Vinciguerra A.Autofluorescence and indocyanine green in thyroid surgery: a systematic review and meta-analysis.Laryngoscope2021;131:1683-92

[53] Bunch PM.Preoperative imaging techniques in primary hyperparathyroidism: a review.JAMA Otolaryngol Head Neck Surg2018;144:929-37

[54] De Feo ML,Biagini C.Parathyroid glands: combination of (99m)Tc MIBI scintigraphy and US for demonstration of parathyroid glands and nodules.Radiology2000;214:393-402

[55] Haber RS,Inabnet WB.Ultrasonography for preoperative localization of enlarged parathyroid glands in primary hyperparathyroidism: comparison with (99m) technetium sestamibi scintigraphy.Clin Endocrinol2002;57:241-9

[56] Hamidi M,Hunter G.4D-CT is superior to ultrasound and Sestamibi for localizing recurrent parathyroid disease.Ann Surg Oncol2018;25:1403-9

[57] McWade MA,Broome JT,Mahadevan-Jansen A.Establishing the clinical utility of autofluorescence spectroscopy for parathyroid detection.Surgery2016;159:193-202 PMCID:PMC4836056

[58] Norlén O,Tay YK.No need to abandon focused parathyroidectomy: a multicenter study of long-term outcome after surgery for primary hyperparathyroidism.Ann Surg2015;261:991-6

[59] Kose E,Aydin H,Berber E.Heterogeneous and low-intensity parathyroid autofluorescence: patterns suggesting hyperfunction at parathyroid exploration.Surgery2019;165:431-7

[60] Demarchi MS,Bédat B,Triponez F.Autofluorescence pattern of parathyroid adenomas.BJS Open2021;5 PMCID:PMC7893478

[61] Chakedis JM,Brumund KT.Indocyanine green fluorescence-guided redo parathyroidectomy.BMJ Case Rep2015;2015:bcr2015211778 PMCID:PMC4567763

[62] DeLong JC,Lwin TM.Indocyanine green fluorescence-guided parathyroidectomy for primary hyperparathyroidism.Surgery2018;163:388-92

[63] Meo G, Karampinis I, Gerken A, Lammert A, Pellicani S, Nowak K. Indocyanine green fluorescence angiography can guide intraoperative localization during parathyroid surgery.Scand J Surg2021;110:59-65

[64] Sound S,Yigitbas H,Berber E.Utility of indocyanine green fluorescence imaging for intraoperative localization in reoperative parathyroid surgery.Surg Innov2019;26:774-9

[65] Zaidi N,Okoh A,Yigitbas H.The utility of indocyanine green near infrared fluorescent imaging in the identification of parathyroid glands during surgery for primary hyperparathyroidism.J Surg Oncol2016;113:771-4

[66] Cui L,Yu H.Intraoperative parathyroid localization with near-infrared fluorescence imaging using indocyanine green during total parathyroidectomy for secondary hyperparathyroidism.Sci Rep2017;7:8193 PMCID:PMC5557759

[67] Fortuny J, Guigard S, Diaper J, Karenovics W, Triponez F. Subtotal parathyroidectomy under indocyanine green angiography.VideoEndocrinology2016;3 PMCID:PMC6961799

[68] Avci SN,Berber E.A visual deep learning model to localize parathyroid-specific autofluorescence on near-infrared imaging : localization of parathyroid autofluorescence with deep learning.Ann Surg Oncol2022:4248-52

[69] Crawford KL,Lee YJ.A scoping review of ongoing fluorescence-guided surgery clinical trials in otolaryngology.Laryngoscope2022;132:36-44