Application of indocyanine green fluorescence imaging in determining blood supply of parathyroid glands during thyroid surgery_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

FEI Yuan , ZHAO Wanjun ,  SU Anping ,  ZHU Jingqiang , LI Zhihui , WEI Tao

Department of Thyroid and Parathyroid Surgery, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding?author：

SU Anping, Email: suanpingping@126.com; ZHU Jingqiang, Email: zjq-wkys@163.com

Keywords：

indocyanine green; fluorescence imaging; blood supply of parathyroid; hypoparathyroidism

DOI：

10.7507/1007-9424.201912024

Video：

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Objective To investigate the application value of indocyanine green (ICG) fluorescence imaging technology for determining the blood supply of parathyroid in thyroid surgery.Methods The patients who underwent total thyroidectomy and bilateral central lymph node dissection for papillary thyroid carcinoma (PTC) from June 1, 2017 to January 1, 2018 were prospectively enrolled and then divided into a study group and control group randomly. The study group used the ICG fluorescence imaging technology to evaluate the blood supply of the parathyroid glands, while the control group assessed the blood supply by naked eyes, then determined that whether the parathyroid glands were retained in situ or autotransplanted. The incidence of hypoparathyroidism, length of hospital stay, and parathyroid hormone (PTH) were compared between the two groups.Results ① A total of 60 patients with PTC were included in the study, and 30 patients in each group. There were no significant differences in the baseline informations of the two groups such as the gender, age, comorbidities, and preoperative PTH, Ca²⁺ levels, etc. (P>0.05). ② The ICG score of type A parathyroid glands (except type A3) was lower than that of type B parathyroid glands (0.99±0.38 versus 1.45±0.58, t=–2.395, P<0.05). ③ The length of postoperative hospital stay was shorter in the study group than in the control group (t=–2.159, P=0.035). ④ The ICG fluorescence imaging could significantly reduce the incidence of temporary hypoparathyroidism (χ²=5.079, P=0.024). The incidence of permanent hypoparathyroidism was not statistically different between the two groups (χ²=1.000, P=0.317), and only 1 case appeared in the control group. ⑤ There were no statistically significant differences in the PTH and serum Ca²⁺ levels at day 1, month 1, month 3, and month 6 after the surgery between the two groups (P>0.05). Conclusion ICG fluorescence imaging technology could be used to determine blood supply of parathyroid in situ in real time during operation. Further studies are needed to confirm this conclusion.

Citation： FEI Yuan, ZHAO Wanjun, SU Anping, ZHU Jingqiang, LI Zhihui, WEI Tao. Application of indocyanine green fluorescence imaging in determining blood supply of parathyroid glands during thyroid surgery. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(9): 1094-1099. doi: 10.7507/1007-9424.201912024 Copy

1.	Zaidi N, Bucak E, Yazici P, et al. The feasibility of indocyanine green fluorescence imaging for identifying and assessing the perfusion of parathyroid glands during total thyroidectomy. J Surg Oncol, 2016, 113(7): 775-778.
2.	Vidal Fortuny J, Belfontali V, Sadowski SM, et al. Parathyroid gland angiography with indocyanine green fluorescence to predict parathyroid function after thyroid surgery. Br J Surg, 2016, 103(5): 537-543.
3.	Rudin AV, McKenzie TJ, Thompson GB, et al. Evaluation of parathyroid glands with indocyanine green fluorescence angiography after thyroidectomy. World J Surg, 2019, 43(6): 1538-1543.
4.	中華醫學會內分泌學分會. 甲狀腺結節和分化型甲狀腺癌診治指南. 中國腫瘤臨床, 2012, 39(17): 1249-1272.
5.	Vidal Fortuny J, Sadowski SM, Belfontali V, et al. Indocyanine green angiography in subtotal parathyroidectomy: Technique for the function of the parathyroid remnant. J Am Coll Surg, 2016, 223(5): e43-e49.
6.	Tartaglia F, Blasi S, Giuliani A, et al. Parathyroid autotransplantation during total thyroidectomy. Results of a retrospective study. Int J Surg, 2016, 28 Suppl 1: S79-S83.
7.	Stack BC Jr, Bimston DN, Bodenner DL, et al. American Association of Clinical Endocrinologists and American College of Endocrinology Disease State Clinical Review: Postoperative hypoparathyroidism—Definitions and management. Endocr Pract, 2015, 21(6): 674-685.
8.	Almquist M, Hallgrimsson P, Nordenstr?m E, et al. Prediction of permanent hypoparathyroidism after total thyroidectomy. World J Surg, 2014, 38(10): 2613-2620.
9.	Asari R, Passler C, Kaczirek K, et al. Hypoparathyroidism after total thyroidectomy: a prospective study. Arch Surg, 2008, 143(2): 132-138.
10.	Sadowski SM, Vidal Fortuny J, Triponez F. A reappraisal of vascular anatomy of the parathyroid gland based on fluorescence techniques. Gland Surg, 2017, 6(Suppl 1): S30-S37.
11.	Johansson K, Ander S, Lennquist S, et al. Human parathyroid blood supply determined by laser-Doppler flowmetry. World J Surg, 1994, 18(3): 417-421.
12.	Kuriloff DB, Kizhner V. Parathyroid gland preservation and selective autotransplantation utilizing topical lidocaine in total thyroidectomy. Laryngoscope, 2010, 120(7): 1342-1344.
13.	易哲福, 李三榮. 2% 利多卡因局部封閉甲狀旁腺周圍對甲狀旁腺功能減退癥的影響. 河北醫藥, 2017, 39(23): 3542-3545.
14.	Ander S, Johansson K, Smeds S. In situ preservation of the parathyroid glands during operations on the Thyroid. Eur J Surg, 1997, 163(1): 33-37.
15.	馬云海, 錢軍, 李書聆, 等. 內鏡觀察術中原位保留甲狀旁腺可行性研究. 中國實用外科雜志, 2016, 36(5): 543-546.
16.	Chakedis JM, Maser C, Brumund KT, et al. Indocyanine green fluorescence-guided redo parathyroidectomy. BMJ Case Rep, 2015, 2015: pii: bcr2015211778.
17.	Suh YJ, Choi JY, Chai YJ, et al. Indocyanine green as a near-infrared fluorescent agent for identifying parathyroid glands during thyroid surgery in dogs. Surg Endosc, 2015, 29(9): 2811-2817.
18.	Jin H, Dong Q, He Z, et al. Application of a fluorescence imaging system with indocyanine green to protect the parathyroid gland intraoperatively and to predict postoperative parathyroidism. Adv Ther, 2018, 35(12): 2167-2175.
19.	Kahramangil B, Berber E. The use of near-infrared fluorescence imaging in endocrine surgical procedures. J Surg Oncol, 2017, 115(7): 848-855.
20.	van den Bos J, van Kooten L, Engelen SME, et al. Feasibility of indocyanine green fluorescence imaging for intraoperative identification of parathyroid glands during thyroid surgery. Head Neck, 2019, 41(2): 340-348.
21.	Kahramangil B, Berber E. Comparison of indocyanine green fluorescence and parathyroid autofluorescence imaging in the identification of parathyroid glands during thyroidectomy. Gland Surg, 2017, 6(6): 644-648.
22.	Vidal Fortuny J, Sadowski SM, Belfontali V, et al. Randomized clinical trial of intraoperative parathyroid gland angiography with indocyanine green fluorescence predicting parathyroid function after thyroid surgery. Br J Surg, 2018, 105(4): 350-357.
23.	Gálvez-Pastor S, Torregrosa NM, Ríos A, et al. Prediction of hypocalcemia after total thyroidectomy using indocyanine green angiography of parathyroid glands: A simple quantitative scoring system. Am J Surg, 2019, 218(5): 993-999.
24.	Llorente PM, Francos Martínez JM, Barrasa AG. Intraoperative parathyroid hormone measurement vs indocyanine green angiography of parathyroid glands in prediction of early postthyroidectomy hypocalcemia. JAMA Surg, 2019 Oct 16. doi: 10.1001/jamasurg.2019.3652.
25.	王彬, 蘇安平, 姜可, 等. 甲狀旁腺分型在評估甲狀旁腺原位保留難易程度中的應用. 中國普外基礎與臨床雜志, 2017, 24(4): 458-463.

1. Zaidi N, Bucak E, Yazici P, et al. The feasibility of indocyanine green fluorescence imaging for identifying and assessing the perfusion of parathyroid glands during total thyroidectomy. J Surg Oncol, 2016, 113(7): 775-778.
2. Vidal Fortuny J, Belfontali V, Sadowski SM, et al. Parathyroid gland angiography with indocyanine green fluorescence to predict parathyroid function after thyroid surgery. Br J Surg, 2016, 103(5): 537-543.
3. Rudin AV, McKenzie TJ, Thompson GB, et al. Evaluation of parathyroid glands with indocyanine green fluorescence angiography after thyroidectomy. World J Surg, 2019, 43(6): 1538-1543.
4. 中華醫學會內分泌學分會. 甲狀腺結節和分化型甲狀腺癌診治指南. 中國腫瘤臨床, 2012, 39(17): 1249-1272.
5. Vidal Fortuny J, Sadowski SM, Belfontali V, et al. Indocyanine green angiography in subtotal parathyroidectomy: Technique for the function of the parathyroid remnant. J Am Coll Surg, 2016, 223(5): e43-e49.
6. Tartaglia F, Blasi S, Giuliani A, et al. Parathyroid autotransplantation during total thyroidectomy. Results of a retrospective study. Int J Surg, 2016, 28 Suppl 1: S79-S83.
7. Stack BC Jr, Bimston DN, Bodenner DL, et al. American Association of Clinical Endocrinologists and American College of Endocrinology Disease State Clinical Review: Postoperative hypoparathyroidism—Definitions and management. Endocr Pract, 2015, 21(6): 674-685.
8. Almquist M, Hallgrimsson P, Nordenstr?m E, et al. Prediction of permanent hypoparathyroidism after total thyroidectomy. World J Surg, 2014, 38(10): 2613-2620.
9. Asari R, Passler C, Kaczirek K, et al. Hypoparathyroidism after total thyroidectomy: a prospective study. Arch Surg, 2008, 143(2): 132-138.
10. Sadowski SM, Vidal Fortuny J, Triponez F. A reappraisal of vascular anatomy of the parathyroid gland based on fluorescence techniques. Gland Surg, 2017, 6(Suppl 1): S30-S37.
11. Johansson K, Ander S, Lennquist S, et al. Human parathyroid blood supply determined by laser-Doppler flowmetry. World J Surg, 1994, 18(3): 417-421.
12. Kuriloff DB, Kizhner V. Parathyroid gland preservation and selective autotransplantation utilizing topical lidocaine in total thyroidectomy. Laryngoscope, 2010, 120(7): 1342-1344.
13. 易哲福, 李三榮. 2% 利多卡因局部封閉甲狀旁腺周圍對甲狀旁腺功能減退癥的影響. 河北醫藥, 2017, 39(23): 3542-3545.
14. Ander S, Johansson K, Smeds S. In situ preservation of the parathyroid glands during operations on the Thyroid. Eur J Surg, 1997, 163(1): 33-37.
15. 馬云海, 錢軍, 李書聆, 等. 內鏡觀察術中原位保留甲狀旁腺可行性研究. 中國實用外科雜志, 2016, 36(5): 543-546.
16. Chakedis JM, Maser C, Brumund KT, et al. Indocyanine green fluorescence-guided redo parathyroidectomy. BMJ Case Rep, 2015, 2015: pii: bcr2015211778.
17. Suh YJ, Choi JY, Chai YJ, et al. Indocyanine green as a near-infrared fluorescent agent for identifying parathyroid glands during thyroid surgery in dogs. Surg Endosc, 2015, 29(9): 2811-2817.
18. Jin H, Dong Q, He Z, et al. Application of a fluorescence imaging system with indocyanine green to protect the parathyroid gland intraoperatively and to predict postoperative parathyroidism. Adv Ther, 2018, 35(12): 2167-2175.
19. Kahramangil B, Berber E. The use of near-infrared fluorescence imaging in endocrine surgical procedures. J Surg Oncol, 2017, 115(7): 848-855.
20. van den Bos J, van Kooten L, Engelen SME, et al. Feasibility of indocyanine green fluorescence imaging for intraoperative identification of parathyroid glands during thyroid surgery. Head Neck, 2019, 41(2): 340-348.
21. Kahramangil B, Berber E. Comparison of indocyanine green fluorescence and parathyroid autofluorescence imaging in the identification of parathyroid glands during thyroidectomy. Gland Surg, 2017, 6(6): 644-648.
22. Vidal Fortuny J, Sadowski SM, Belfontali V, et al. Randomized clinical trial of intraoperative parathyroid gland angiography with indocyanine green fluorescence predicting parathyroid function after thyroid surgery. Br J Surg, 2018, 105(4): 350-357.
23. Gálvez-Pastor S, Torregrosa NM, Ríos A, et al. Prediction of hypocalcemia after total thyroidectomy using indocyanine green angiography of parathyroid glands: A simple quantitative scoring system. Am J Surg, 2019, 218(5): 993-999.
24. Llorente PM, Francos Martínez JM, Barrasa AG. Intraoperative parathyroid hormone measurement vs indocyanine green angiography of parathyroid glands in prediction of early postthyroidectomy hypocalcemia. JAMA Surg, 2019 Oct 16. doi: 10.1001/jamasurg.2019.3652.
25. 王彬, 蘇安平, 姜可, 等. 甲狀旁腺分型在評估甲狀旁腺原位保留難易程度中的應用. 中國普外基礎與臨床雜志, 2017, 24(4): 458-463.

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Application of indocyanine green fluorescence imaging in determining blood supply of parathyroid glands during thyroid surgery

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