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Published in: Surgical Endoscopy 9/2015

01-09-2015 | Dynamic Manuscript

Indocyanine green as a near-infrared fluorescent agent for identifying parathyroid glands during thyroid surgery in dogs

Authors: Yong Joon Suh, June Young Choi, Young Jun Chai, Hyungju Kwon, Jung-Woo Woo, Su-jin Kim, Kyu Hyung Kim, Kyu Eun Lee, Yong Taik Lim, Yeo-Kyu Youn

Published in: Surgical Endoscopy | Issue 9/2015

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Abstract

Background

Surgical procedures involving the thyroid gland require identification of the parathyroid glands. Indocyanine green (ICG) is a near-infrared (NIR) fluorescent contrast agent used for a variety of procedures such as intraoperative angiography, extrahepatic cholangiography, and lymph node mapping. In this study, we used a canine model to evaluate ICG for NIR fluorescent imaging of the parathyroid gland.

Methods

Three dogs were used for the study. The dogs were administered general anesthesia, and after surgical dissection, each dog received a series of intravenous ICG doses ranging from 12.5 to 100 µg/kg ICG. The excitation light source used to illuminate the operating field was a NIR laser (λ = 785 nm). Intravascular ICG fluorescence (λ = 835/45 nm) was recorded using a charge-coupled device that employed optical filtering to block ambient and laser light. Fluorescent imaging was assessed after injection of each dose of ICG.

Results

NIR fluorescent imaging visualized the parathyroid glands. The intensity curves showing the peak and plateau of fluorescence are similar regardless of the concentration of ICG. The time to peak fluorescent intensity was 50.2 ± 2.0 s after injection of ICG. Taking into consideration background fluorescent intensity, the estimated optimal dose of ICG was 18.75 µg/kg. At 106.7 ± 5.8 s, the parathyroid glands lost much of their fluorescence, although they remained sufficiently fluorescent to be distinguishable. There was a positive correlation of fluorescent intensity with ICG dose escalation up to 25 µg/kg.

Conclusions

ICG NIR fluorescent imaging was useful in detecting the parathyroid glands of dogs. By allowing detection of parathyroid glands, the current technique shows promise for use by endocrine surgeons performing thyroidectomies.
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Literature
1.
go back to reference Myriam L, Ralph PT, Christine GG (2013) National trends in thyroid surgery and the effect of volume on short-term outcomes. Laryngoscope 123(8):2056–2063CrossRef Myriam L, Ralph PT, Christine GG (2013) National trends in thyroid surgery and the effect of volume on short-term outcomes. Laryngoscope 123(8):2056–2063CrossRef
2.
go back to reference George HS, Vania S, Constantinos B, Nikolaos K, Theophilos K, George K (2005) Incidental parathyroidectomy during thyroid surgery: an underappreciated complication of thyroidectomy. World J Surg 29(12):1539–1543CrossRef George HS, Vania S, Constantinos B, Nikolaos K, Theophilos K, George K (2005) Incidental parathyroidectomy during thyroid surgery: an underappreciated complication of thyroidectomy. World J Surg 29(12):1539–1543CrossRef
3.
go back to reference Marshall MV, Rasmussen JC, Tan IC, Aldrich MB, Adams KE, Wang X, Fife CE, Maus EA, Smith LA, Sevick-Muraca EM (2010) Near-infrared fluorescence imaging in humans with indocyanine green: a review and update. Open Surg Oncol J 2(2):12–25PubMedCentralCrossRefPubMed Marshall MV, Rasmussen JC, Tan IC, Aldrich MB, Adams KE, Wang X, Fife CE, Maus EA, Smith LA, Sevick-Muraca EM (2010) Near-infrared fluorescence imaging in humans with indocyanine green: a review and update. Open Surg Oncol J 2(2):12–25PubMedCentralCrossRefPubMed
4.
go back to reference Miwa M (2010) The principle of ICG fluorescence method. Open Surg Oncol J 2:26–28CrossRef Miwa M (2010) The principle of ICG fluorescence method. Open Surg Oncol J 2:26–28CrossRef
5.
go back to reference Alander JT, Kaartinen I, Laakso A, Pätilä T, Spillmann T, Tuchin VV, Venermo M, Välisuo P (2012) A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012:940585PubMedCentralCrossRefPubMed Alander JT, Kaartinen I, Laakso A, Pätilä T, Spillmann T, Tuchin VV, Venermo M, Välisuo P (2012) A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012:940585PubMedCentralCrossRefPubMed
6.
go back to reference Noh YW, Kong SH, Choi DY, Park HS, Yang HK, Lee HJ, Kim HC, Kang KW, Sung MH, Lim YT (2012) Near-infrared emitting polymer nanogels for efficient sentinel lymph node mapping. ACS Nano 6(9):7820–7831CrossRefPubMed Noh YW, Kong SH, Choi DY, Park HS, Yang HK, Lee HJ, Kim HC, Kang KW, Sung MH, Lim YT (2012) Near-infrared emitting polymer nanogels for efficient sentinel lymph node mapping. ACS Nano 6(9):7820–7831CrossRefPubMed
7.
go back to reference Evans HE, DeLahunta A (2013) Miller’s anatomy of the dog, 4th edn. W. B. Saunders, St. Louis Evans HE, DeLahunta A (2013) Miller’s anatomy of the dog, 4th edn. W. B. Saunders, St. Louis
9.
go back to reference Han N, Bumpous JM, Goldstein RE, Fleming MM, Flynn MB (2007) Intra-operative parathyroid identification using methylene blue in parathyroid surgery. Am Surg 73(8):820–823PubMed Han N, Bumpous JM, Goldstein RE, Fleming MM, Flynn MB (2007) Intra-operative parathyroid identification using methylene blue in parathyroid surgery. Am Surg 73(8):820–823PubMed
10.
go back to reference Patel HP, Chadwick DR, Harrison BJ, Balasubramanian SP (2012) Systematic review of intravenous methylene blue in parathyroid surgery. Br J Surg 99(10):1345–1351CrossRefPubMed Patel HP, Chadwick DR, Harrison BJ, Balasubramanian SP (2012) Systematic review of intravenous methylene blue in parathyroid surgery. Br J Surg 99(10):1345–1351CrossRefPubMed
11.
go back to reference Pollack G, Pollack A, Delfiner J, Fernandez J (2009) Parathyroid surgery and methylene blue: a review with guidelines for safe intraoperative use. Laryngoscope 119(10):1941–1946CrossRefPubMed Pollack G, Pollack A, Delfiner J, Fernandez J (2009) Parathyroid surgery and methylene blue: a review with guidelines for safe intraoperative use. Laryngoscope 119(10):1941–1946CrossRefPubMed
12.
go back to reference Grubbs EG, Mittendorf EA, Perrier ND, Lee JE (2008) Gamma probe identification of normal parathyroid glands during central neck surgery can facilitate parathyroid preservation. Am J Surg 196(6):931–935 discussion 935-6CrossRefPubMed Grubbs EG, Mittendorf EA, Perrier ND, Lee JE (2008) Gamma probe identification of normal parathyroid glands during central neck surgery can facilitate parathyroid preservation. Am J Surg 196(6):931–935 discussion 935-6CrossRefPubMed
13.
go back to reference Suzuki T, Numata T, Shibuya M (2011) Intraoperative photodynamic detection of normal parathyroid glands using 5-aminolevulinic acid. Laryngoscope 121(7):1462–1466CrossRefPubMed Suzuki T, Numata T, Shibuya M (2011) Intraoperative photodynamic detection of normal parathyroid glands using 5-aminolevulinic acid. Laryngoscope 121(7):1462–1466CrossRefPubMed
14.
go back to reference Asher SA, Peters GE, Pehler SF, Zinn K, Newman JR, Rosenthal EL (2008) Fluorescent detection of rat parathyroid glands via 5-aminolevulinic acid. Laryngoscope 118(6):1014–1018CrossRefPubMed Asher SA, Peters GE, Pehler SF, Zinn K, Newman JR, Rosenthal EL (2008) Fluorescent detection of rat parathyroid glands via 5-aminolevulinic acid. Laryngoscope 118(6):1014–1018CrossRefPubMed
15.
go back to reference Paras C, Keller M, White L, Phay J, Mahadevan-Jansen A (2011) Near-infrared autofluorescence for the detection of parathyroid glands. J Biomed Opt 16(6):067012CrossRefPubMed Paras C, Keller M, White L, Phay J, Mahadevan-Jansen A (2011) Near-infrared autofluorescence for the detection of parathyroid glands. J Biomed Opt 16(6):067012CrossRefPubMed
16.
go back to reference Desmettre T, Devoisselle JM, Mordon S (2000) Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography. Surv Ophthalmol 45(1):15–27CrossRefPubMed Desmettre T, Devoisselle JM, Mordon S (2000) Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography. Surv Ophthalmol 45(1):15–27CrossRefPubMed
17.
go back to reference van den Biesen PR, Jongsma FH, Tangelder GJ, Slaaf DW (1995) Yield of fluorescence from indocyanine green in plasma and flowing blood. Ann Biomed Eng 23(4):475–481CrossRefPubMed van den Biesen PR, Jongsma FH, Tangelder GJ, Slaaf DW (1995) Yield of fluorescence from indocyanine green in plasma and flowing blood. Ann Biomed Eng 23(4):475–481CrossRefPubMed
18.
go back to reference Maarek JMI, Holschneider DP (2009) Estimation of indocyanine green concentration in blood from fluorescence emission: application to hemodynamic assessment during hemodialysis. J Biomed Opt 14(5):054006CrossRefPubMed Maarek JMI, Holschneider DP (2009) Estimation of indocyanine green concentration in blood from fluorescence emission: application to hemodynamic assessment during hemodialysis. J Biomed Opt 14(5):054006CrossRefPubMed
19.
go back to reference Kang SW, Park JH, Jeong JS, Lee CR, Park S, Lee SH, Jeong JJ, Nam KH, Chung WY, Park CS (2011) Prospects of robotic thyroidectomy using a gasless, transaxillary approach for the management of thyroid carcinoma. Surg Laparosc Endosc Percutan Tech 21(4):223–229CrossRefPubMed Kang SW, Park JH, Jeong JS, Lee CR, Park S, Lee SH, Jeong JJ, Nam KH, Chung WY, Park CS (2011) Prospects of robotic thyroidectomy using a gasless, transaxillary approach for the management of thyroid carcinoma. Surg Laparosc Endosc Percutan Tech 21(4):223–229CrossRefPubMed
20.
go back to reference Giordano D, Valcavi R, Thompson GB, Pedroni C, Renna L, Gradoni P, Barbieri V (2012) Complications of central neck dissection in patients with papillary thyroid carcinoma: results of a study on 1087 patients and review of the literature. Thyroid 22(9):911–917CrossRefPubMed Giordano D, Valcavi R, Thompson GB, Pedroni C, Renna L, Gradoni P, Barbieri V (2012) Complications of central neck dissection in patients with papillary thyroid carcinoma: results of a study on 1087 patients and review of the literature. Thyroid 22(9):911–917CrossRefPubMed
21.
go back to reference Lee KE, Kim E, Koo do H, Choi JY, Kim KH, Youn YK (2013) Robotic thyroidectomy by bilateral axillo-breast approach: review of 1,026 cases and surgical completeness. Surg Endosc 27(8):2955–2962CrossRefPubMed Lee KE, Kim E, Koo do H, Choi JY, Kim KH, Youn YK (2013) Robotic thyroidectomy by bilateral axillo-breast approach: review of 1,026 cases and surgical completeness. Surg Endosc 27(8):2955–2962CrossRefPubMed
22.
go back to reference Yi O, Yoon JH, Lee YM, Sung TY, Chung KW, Kim TY, Kim WB, Shong YK, Ryu JS, Hong SJ (2013) Technical and oncologic safety of robotic thyroid surgery. Ann Surg Oncol 20(6):1927–1933CrossRefPubMed Yi O, Yoon JH, Lee YM, Sung TY, Chung KW, Kim TY, Kim WB, Shong YK, Ryu JS, Hong SJ (2013) Technical and oncologic safety of robotic thyroid surgery. Ann Surg Oncol 20(6):1927–1933CrossRefPubMed
23.
go back to reference Jackson NR, Yao L, Tufano RP, Kandil EH (2013) Safety of robotic thyroidectomy approaches: meta-analysis and systematic review. Head Neck. doi:10.1002/hed.23223 Jackson NR, Yao L, Tufano RP, Kandil EH (2013) Safety of robotic thyroidectomy approaches: meta-analysis and systematic review. Head Neck. doi:10.​1002/​hed.​23223
24.
go back to reference Lee J, Kwon IS, Bae EH, Chung WY (2013) Comparative analysis of oncological outcomes and quality of life after robotic versus conventional open thyroidectomy with modified radical neck dissection in patients with papillary thyroid carcinoma and lateral neck node metastases. J Clin Endocrinol Metab 98(7):2701–2708CrossRefPubMed Lee J, Kwon IS, Bae EH, Chung WY (2013) Comparative analysis of oncological outcomes and quality of life after robotic versus conventional open thyroidectomy with modified radical neck dissection in patients with papillary thyroid carcinoma and lateral neck node metastases. J Clin Endocrinol Metab 98(7):2701–2708CrossRefPubMed
25.
go back to reference Wagner OJ, Louie BE, Vallieres E, Aye RW, Farivar AS (2012) Near-infrared fluorescence imaging can help identify the contralateral phrenic nerve during robotic thymectomy. Ann Thorac Surg 94(2):622–625CrossRefPubMed Wagner OJ, Louie BE, Vallieres E, Aye RW, Farivar AS (2012) Near-infrared fluorescence imaging can help identify the contralateral phrenic nerve during robotic thymectomy. Ann Thorac Surg 94(2):622–625CrossRefPubMed
26.
go back to reference Angell JE, Khemees TA, Abaza R (2013) Optimization of near infrared fluorescence tumor localization during robotic partial nephrectomy. J Urol 190(5):1668–1673CrossRefPubMed Angell JE, Khemees TA, Abaza R (2013) Optimization of near infrared fluorescence tumor localization during robotic partial nephrectomy. J Urol 190(5):1668–1673CrossRefPubMed
27.
go back to reference Schols RM, Bouvy ND, van Dam RM, Stassen LP (2013) Advanced intraoperative imaging methods for laparoscopic anatomy navigation: an overview. Surg Endosc 27(6):1851–1859CrossRefPubMed Schols RM, Bouvy ND, van Dam RM, Stassen LP (2013) Advanced intraoperative imaging methods for laparoscopic anatomy navigation: an overview. Surg Endosc 27(6):1851–1859CrossRefPubMed
Metadata
Title
Indocyanine green as a near-infrared fluorescent agent for identifying parathyroid glands during thyroid surgery in dogs
Authors
Yong Joon Suh
June Young Choi
Young Jun Chai
Hyungju Kwon
Jung-Woo Woo
Su-jin Kim
Kyu Hyung Kim
Kyu Eun Lee
Yong Taik Lim
Yeo-Kyu Youn
Publication date
01-09-2015
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 9/2015
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-014-3971-2

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