Evaluation of blood perfusion of parathyroid glands by indocyanine green fluorescence imaging during total thyroidectomy_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

PI Qifei ^1,2 , YIN Supeng ¹ , SUN Yiceng ¹ , PAN Bin ¹ ,  ZHANG Fan ¹

1. Department of Breast and Thyroid Surgery, Chongqing General Hospital, Chongqing 401121, P. R. China;
2. Department of Thoracic, Thyroid, and Breast Surgery, People’s Hospital of Anshun City, Anshun, Guizhou 561099, P. R. China;

Corresponding?author：

ZHANG Fan, Email: zhangfancgh@163.com

Keywords：

indocyanine green fluorescence imaging; blood perfusion of parathyroid gland; total thyroidectomy; hypoparathyroidism

DOI：

10.7507/1007-9424.202206021

Video：

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Objective To explore the accuracy and efficiency of indocyanine green fluorescence (ICGF) imaging in evaluating blood perfusion of parathyroid gland (PG) during total thyroidectomy. Methods Seventy patients who underwent total thyroidectomy and bilateral central lymph node dissection for papillary thyroid carcinoma (PTC) from March 2021 to December 2021 were enrolled and randomly divided into experimental group (ICGF imaging, n=35) and control group (normal treatment, n=35). Blood perfusion of PGs was evaluated by ICGF imaging and naked eye in each group respectively. The perfusion of PGs, incidence of hypoparathyroidism, and number of autotransplanted PGs were analyzed between the two groups. Results There was no difference between two groups in the incidence of transient hypoparathyroidism (P=0.339), and no one occurred permanent hypoparathyroidism. More PGs were autotransplanted in the experimental group compared to the control group (P＜0.001). At least one PG with good perfusion in the experimental group predicted an extremely high rate of normal parathyroid hormone levels of the patients postoperatively than the control group (P=0.003). Conclusion ICGF imaging can evaluate the blood perfusion of PGs accurately and guide their autotransplantation.

Citation： PI Qifei, YIN Supeng, SUN Yiceng, PAN Bin, ZHANG Fan. Evaluation of blood perfusion of parathyroid glands by indocyanine green fluorescence imaging during total thyroidectomy. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(10): 1313-1317. doi: 10.7507/1007-9424.202206021 Copy

1.	鄭榮壽, 孫可欣, 張思維, 等. 2015年中國惡性腫瘤流行情況分析. 中華腫瘤雜志, 2019, 41(1): 19-28.
2.	Zheng R, Zhang S, Zeng H, et al. Cancer incidence and mortality in China, 2016. J Natl Cancer Cent, 2022, 2(1): 1-9.
3.	Rosato L, Avenia N, Bernante P, et al. Complications of thyroid surgery: analysis of a multicentric study on 14 934 patients operated on in Italy over 5 years. World J Surg, 2004, 28(3): 271-276.
4.	Efremidou EI, Papageorgiou MS, Liratzopoulos N, et al. The efficacy and safety of total thyroidectomy in the management of benign thyroid disease: a review of 932 cases. Can J Surg, 2009, 52(1): 39-44.
5.	Christou N, Mathonnet M. Complications after total thyroidectomy. J Visc Surg, 2013, 150(4): 249-256.
6.	Edafe O, Antakia R, Laskar N, et al. Systematic review and meta-analysis of predictors of post-thyroidectomy hypocalcaemia. Br J Surg, 2014, 101(4): 307-320.
7.	Bilezikian JP, Khan A, Potts JT Jr, et al. Hypoparathyroidism in the adult: epidemiology, diagnosis, pathophysiology, target-organ involvement, treatment, and challenges for future research. J Bone Miner Res, 2011, 26(10): 2317-2337.
8.	Testini M, Rosato L, Avenia N, et al. The impact of single parathyroid gland autotransplantation during thyroid surgery on postoperative hypoparathyroidism: a multicenter study. Transplant Proc, 2007, 39(1): 225-230.
9.	Iorio O, Petrozza V, De Gori A, et al. Parathyroid autotransplantation during thyroid surgery. Where we are? A systematic review on indications and results. J Invest Surg, 2019, 32(7): 594-601.
10.	Hicks G, George R, Sywak M. Short and long-term impact of parathyroid autotransplantation on parathyroid function after total thyroidectomy. Gland Surg, 2017, 6(Suppl 1): S75-S85. doi: 10.21037/gs.2017.09.15.
11.	Abbaci M, De Leeuw F, Breuskin I, et al. Parathyroid gland management using optical technologies during thyroidectomy or parathyroidectomy: a systematic review. Oral Oncol, 2018, 87: 186-196.
12.	Spartalis E, Ntokos G, Georgiou K, et al. Intraoperative indocyanine green (ICG) angiography for the identification of the parathyroid glands: current evidence and future perspectives. In Vivo, 2020, 34(1): 23-32.
13.	Wong A, Wong JCY, Pandey PU, et al. Novel techniques for intraoperative parathyroid gland identification: a comprehensive review. Expert Rev Endocrinol Metab, 2020, 15(6): 439-457.
14.	Barbieri D, Indelicato P, Vinciguerra A, et al. Autofluorescence and indocyanine green in thyroid surgery: a systematic review and meta-analysis. Laryngoscope, 2021, 131(7): 1683-1692.
15.	American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid, 2009, 19(11): 1167-1214.
16.	中國醫師協會外科醫師分會甲狀腺外科醫師委員會. 甲狀腺手術中甲狀旁腺保護專家共識. 中國實用外科雜志, 2015, 35(7): 731-736.
17.	Song CM, Jung JH, Ji YB, et al. Relationship between hypoparathyroidism and the number of parathyroid glands preserved during thyroidectomy. World J Surg Oncol, 2014, 12(1): 200. doi: 10.1186/1477-7819-12-200.
18.	Abboud B, Sleilaty G, Zeineddine S, et al. Is therapy with calcium and vitamin D and parathyroid autotransplantation useful in total thyroidectomy for preventing hypocalcemia? Head Neck, 2008, 30(9): 1148-1154.
19.	Desmettre T, Devoisselle JM, Mordon S. Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography. Surv Ophthalmol, 2000, 45(1): 15-27.
20.	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.
21.	Lang BH, Wong CK, Hung HT, et al. Indocyanine green fluorescence angiography for quantitative evaluation of in situ parathyroid gland perfusion and function after total thyroidectomy. Surgery, 2017, 161(1): 87-95.
22.	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.
23.	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.
24.	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.
25.	費媛, 趙婉君, 蘇安平, 等. 吲哚菁綠熒光顯像技術在甲狀腺手術中對甲狀旁腺血供判斷的應用. 中國普外基礎與臨床雜志, 2020, 27(9): 1094-1099.

1. 鄭榮壽, 孫可欣, 張思維, 等. 2015年中國惡性腫瘤流行情況分析. 中華腫瘤雜志, 2019, 41(1): 19-28.
2. Zheng R, Zhang S, Zeng H, et al. Cancer incidence and mortality in China, 2016. J Natl Cancer Cent, 2022, 2(1): 1-9.
3. Rosato L, Avenia N, Bernante P, et al. Complications of thyroid surgery: analysis of a multicentric study on 14 934 patients operated on in Italy over 5 years. World J Surg, 2004, 28(3): 271-276.
4. Efremidou EI, Papageorgiou MS, Liratzopoulos N, et al. The efficacy and safety of total thyroidectomy in the management of benign thyroid disease: a review of 932 cases. Can J Surg, 2009, 52(1): 39-44.
5. Christou N, Mathonnet M. Complications after total thyroidectomy. J Visc Surg, 2013, 150(4): 249-256.
6. Edafe O, Antakia R, Laskar N, et al. Systematic review and meta-analysis of predictors of post-thyroidectomy hypocalcaemia. Br J Surg, 2014, 101(4): 307-320.
7. Bilezikian JP, Khan A, Potts JT Jr, et al. Hypoparathyroidism in the adult: epidemiology, diagnosis, pathophysiology, target-organ involvement, treatment, and challenges for future research. J Bone Miner Res, 2011, 26(10): 2317-2337.
8. Testini M, Rosato L, Avenia N, et al. The impact of single parathyroid gland autotransplantation during thyroid surgery on postoperative hypoparathyroidism: a multicenter study. Transplant Proc, 2007, 39(1): 225-230.
9. Iorio O, Petrozza V, De Gori A, et al. Parathyroid autotransplantation during thyroid surgery. Where we are? A systematic review on indications and results. J Invest Surg, 2019, 32(7): 594-601.
10. Hicks G, George R, Sywak M. Short and long-term impact of parathyroid autotransplantation on parathyroid function after total thyroidectomy. Gland Surg, 2017, 6(Suppl 1): S75-S85. doi: 10.21037/gs.2017.09.15.
11. Abbaci M, De Leeuw F, Breuskin I, et al. Parathyroid gland management using optical technologies during thyroidectomy or parathyroidectomy: a systematic review. Oral Oncol, 2018, 87: 186-196.
12. Spartalis E, Ntokos G, Georgiou K, et al. Intraoperative indocyanine green (ICG) angiography for the identification of the parathyroid glands: current evidence and future perspectives. In Vivo, 2020, 34(1): 23-32.
13. Wong A, Wong JCY, Pandey PU, et al. Novel techniques for intraoperative parathyroid gland identification: a comprehensive review. Expert Rev Endocrinol Metab, 2020, 15(6): 439-457.
14. Barbieri D, Indelicato P, Vinciguerra A, et al. Autofluorescence and indocyanine green in thyroid surgery: a systematic review and meta-analysis. Laryngoscope, 2021, 131(7): 1683-1692.
15. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid, 2009, 19(11): 1167-1214.
16. 中國醫師協會外科醫師分會甲狀腺外科醫師委員會. 甲狀腺手術中甲狀旁腺保護專家共識. 中國實用外科雜志, 2015, 35(7): 731-736.
17. Song CM, Jung JH, Ji YB, et al. Relationship between hypoparathyroidism and the number of parathyroid glands preserved during thyroidectomy. World J Surg Oncol, 2014, 12(1): 200. doi: 10.1186/1477-7819-12-200.
18. Abboud B, Sleilaty G, Zeineddine S, et al. Is therapy with calcium and vitamin D and parathyroid autotransplantation useful in total thyroidectomy for preventing hypocalcemia? Head Neck, 2008, 30(9): 1148-1154.
19. Desmettre T, Devoisselle JM, Mordon S. Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography. Surv Ophthalmol, 2000, 45(1): 15-27.
20. 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.
21. Lang BH, Wong CK, Hung HT, et al. Indocyanine green fluorescence angiography for quantitative evaluation of in situ parathyroid gland perfusion and function after total thyroidectomy. Surgery, 2017, 161(1): 87-95.
22. 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.
23. 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.
24. 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.
25. 費媛, 趙婉君, 蘇安平, 等. 吲哚菁綠熒光顯像技術在甲狀腺手術中對甲狀旁腺血供判斷的應用. 中國普外基礎與臨床雜志, 2020, 27(9): 1094-1099.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Evaluation of blood perfusion of parathyroid glands by indocyanine green fluorescence imaging during total thyroidectomy

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