Progress of fluorescence imaging in the study of parathyroid blood supply_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YANG Xiaoqing , WANG Zhengzhai , LIN Xiyuan , LIN Xiangfeng ,  ZHENG Haitao

Department of Thyroid Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong 264000, P. R. China;

Corresponding?author：

ZHENG Haitao, Email: zhenghaitao1972@126.com

Keywords：

parathyroid blood supply; indocyanine green; near-infrared autofluorescence; laser speckle contrast imaging

DOI：

10.7507/1007-9424.202206078

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To understand the methods of judging the blood supply of parathyroid during thyroidectomy at home and abroad in recent years. Method The literature on parathyroid blood supply was collected, the research progress was reviewed, and the advantages and disadvantages of related methods were analyzed. Results In recent years, near-infrared fluorescence, laser speckle contrast imaging and other technologies had been applied. They showed better advantages as compared with naked eye observation. The research on parathyroid blood supply at home and abroad was still in its infancy, and more clinical samples and related equipment optimization were still needed. Conclusion Fluorescence imaging technology has a certain auxiliary role in the judgment of intraoperative parathyroid blood supply and can reduce the incidence of hypoparathyroidism to a certain extent.

Citation： YANG Xiaoqing, WANG Zhengzhai, LIN Xiyuan, LIN Xiangfeng, ZHENG Haitao. Progress of fluorescence imaging in the study of parathyroid blood supply. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(1): 105-109. doi: 10.7507/1007-9424.202206078 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.	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.
3.	Kakava K, Tournis S, Papadakis G, et al. Postsurgical hypoparathyroidism: a systematic review. In Vivo, 2016, 30(3): 171-179.
4.	Park I, Rhu J, Woo JW, et al. Preserving parathyroid gland vasculature to reduce post-thyroidectomy hypocalcemia. World J Surg, 2016, 40(6): 1382-1389.
5.	侯迎晨, 賀晨宇, 賀建業, 等. 小切口腔鏡輔助甲狀腺手術中不同張力操作對上位甲狀旁腺血運的影響. 中國微創外科雜志, 2018, 18(7): 600-603.
6.	Sung TY, Lee YM, Yoon JH, et al. Importance of the intraoperative appearance of preserved parathyroid glands after total thyroidectomy. Surg Today, 2016, 46(3): 356-362.
7.	周東懷, 張瑞廣, 廖斌, 等. 甲狀腺全切除術中對甲狀旁腺特異性附著脂肪進行保護的臨床和解剖分析. 中國醫藥科學, 2018, 8(6): 167-170.
8.	Lang BHH, Chan DTY, Chow FCL, et al. The association of discolored parathyroid glands and hypoparathyroidism following total thyroidectomy. World J Surg, 2016, 40(7): 1611-1617.
9.	Promberger R, Ott J, Kober F, et al. Normal parathyroid hormone levels do not exclude permanent hypoparathyroidism after thyroidectomy. Thyroid, 2011, 21(2): 145-150.
10.	郭飛躍, 耿勝杰, 張靜. 甲狀旁腺自體熒光顯像技術的研究進展. 臨床耳鼻咽喉頭頸外科雜志, 2022, 36(5): 397-401.
11.	宋西成, 鄭海濤. 甲狀旁腺自熒光顯影技術應用研究. 山東大學耳鼻喉眼學報, 2020, 34(3): 19-25.
12.	鄭偉慧, 王可敬. 甲狀腺手術中甲狀旁腺顯影的臨床應用進展. 腫瘤學雜志, 2022, 28(4): 327-331.
13.	Landsman ML, Kwant G, Mook GA, et al. Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol, 1976, 40(4): 575-583.
14.	Alander JT, Kaartinen I, Laakso A, et al. A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging, 2012, 2012: 940585. doi: 10.1155/2012/940585.
15.	吳國聰, 李俊, 徐威, 等. 吲哚菁綠顯像在預防腹腔鏡結直腸癌根治術后吻合口漏中的應用. 西部醫學, 2021, 33(7): 1035-1038.
16.	張寒, 游曉波, 蔡震, 等. 吲哚菁綠熒光造影技術在惡性黑色素瘤前哨淋巴結活檢中的應用探討. 實用醫院臨床雜志, 2020, 17(3): 231-232.
17.	Kahramangil B, Berber E. The use of near-infrared fluorescence imaging in endocrine surgical procedures. J Surg Oncol, 2017, 115(7): 848-855.
18.	張珂, 趙輝, 時琳琳, 等. 吲哚菁綠熒光成像技術在甲狀旁腺和甲狀腺手術中的應用研究進展. 浙江醫學, 2021, 43(20): 2254-2257, 2262.
19.	任正君. 吲哚菁綠(ICG)熒光顯像在甲狀腺手術中保護甲狀旁腺和預測術后低鈣血癥的應用. 河北醫科大學, 2021. doi:10.27111/d.cnki.ghyku.2021.000731.
20.	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.
21.	Lang B HH, Wong CKH, 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.	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.
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.	Vidal Fortuny J, Guigard S, Diaper J, et al. Subtotal parathyroidectomy under indocyanine green angiography. VideoEndocrinology, 2016, 3(1): ve. 2015.0056. doi: 10.1089/ve.2015.0056.
25.	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.
26.	Yavuz E, Biricik A, Karagulle OO, et al. A comparison of the quantitative evaluation of in situ parathyroid gland perfusion by indocyanine green fluorescence angiography and by visual examination in thyroid surgery. Arch Endocrinol Metab, 2020, 64(4): 427-435.
27.	Priyanka S, Sam ST, Rebekah G, et al. The utility of indocyanine green (ICG) for the identification and assessment of viability of the parathyroid glands during thyroidectomy. Updates Surg, 2022, 74(1): 97-105.
28.	Noltes ME, Metman MJH, Heeman W, et al. A novel and generic workflow of indocyanine green perfusion assessment integrating standardization and quantification toward clinical implementation. Ann Surg, 2021, 274(6): e659-e663. doi: 10.1097/SLA.0000000000004978.
29.	Paras C, Keller M, White L, et al. Near-infrared autofluorescence for the detection of parathyroid glands. J Biomed Opt, 2011, 16(6): 067012. doi: 10.1117/1.3583571.
30.	Di Marco AN, Palazzo FF. Near-infrared autofluorescence in thyroid and parathyroid surgery. Gland Surg, 2020, 9(Suppl 2): S136-S146. doi: 10.21037/gs.2020.01.04.
31.	Shinden Y, Nakajo A, Arima H, et al. Intraoperative identification of the parathyroid gland with a fluorescence detection system. World J Surg, 2017, 41(6): 1506-1512.
32.	De Leeuw F, Breuskin I, Abbaci M, et al. Intraoperative near-infrared imaging for parathyroid gland identification by auto-fluorescence: a feasibility study. World J Surg, 2016, 40(9): 2131-2138.
33.	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.
34.	Jin H, Fan J, Yang J, et al. Application of indocyanine green in the parathyroid detection and protection: Report of 3 cases. Am J Otolaryngol, 2019, 40(2): 323-330.
35.	Lerchenberger M, Al Arabi N, Gallwas JKS, et al. Intraoperative near-infrared autofluorescence and indocyanine green imaging to identify parathyroid glands: a comparison. Int J Endocrinol, 2019, 2019: 4687951. doi: 10.1155/2019/4687951.
36.	Parfentiev R, Grubnik V, Grubnik V, et al. Study of intraoperative indocyanine green angiography effectiveness for identification of parathyroid gland during total thyroidectomy. Georgian medical news, 2021, 314: 26-29.
37.	Oh E, Lee HC, Kim Y, et al. A pilot feasibility study to assess vascularity and perfusion of parathyroid glands using a portable hand-held imager. Lasers Surg Med, 2022, 54(3): 399-406.
38.	Lo CY. Parathyroid autotransplantation during thyroidectomy. ANZ J Surg, 2002, 72(12): 902-907.
39.	Aminfar A, Davoodzadeh N, Aguilar G, et al. Application of optical flow algorithms to laser speckle imaging. Microvasc Res, 2019, 122: 52-59.
40.	Heeman W, Steenbergen W, van Dam G, et al. Clinical applications of laser speckle contrast imaging: a review. J Biomed Opt, 2019, 24(8): 1-11.
41.	李鵬程. 生物組織高分辨激光散斑血流成像技術研究. 第八屆全國光生物學學術會議論文摘要集. 2013, 24.
42.	Boas DA, Dunn AK. Laser speckle contrast imaging in biomedical optics. J Biomed Opt, 2010, 15(1): 011109. doi: 10.1117/1.3285504.
43.	To C, Rees-Lee JE, Gush RJ, et al. Intraoperative tissue perfusion measurement by laser speckle imaging: A potential aid for reducing postoperative complications in free flap breast reconstruction. Plast Reconstr Surg, 2019, 143(2): 287e-292e. doi: 10.1097/PRS.0000000000005223.
44.	Mannoh EA, Thomas G, Solórzano CC, et al. Intraoperative assessment of parathyroid viability using laser speckle contrast imaging. Sci Rep, 2017, 7(1): 14798. doi: 10.1038/s41598-017-14941-5.
45.	Mannoh EA, Thomas G, Baregamian N, et al. Assessing intraoperative laser speckle contrast imaging of parathyroid glands in relation to total thyroidectomy patient outcomes. Thyroid, 2021, 31(10): 1558-1565.
46.	Mannoh EA, Parker LB, Thomas G, et al. Development of an imaging device for label-free parathyroid gland identification and vascularity assessment. J Biophotonics, 2021, 14(6): e202100008. doi: 10.1002/jbio.202100008.

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. 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.
3. Kakava K, Tournis S, Papadakis G, et al. Postsurgical hypoparathyroidism: a systematic review. In Vivo, 2016, 30(3): 171-179.
4. Park I, Rhu J, Woo JW, et al. Preserving parathyroid gland vasculature to reduce post-thyroidectomy hypocalcemia. World J Surg, 2016, 40(6): 1382-1389.
5. 侯迎晨, 賀晨宇, 賀建業, 等. 小切口腔鏡輔助甲狀腺手術中不同張力操作對上位甲狀旁腺血運的影響. 中國微創外科雜志, 2018, 18(7): 600-603.
6. Sung TY, Lee YM, Yoon JH, et al. Importance of the intraoperative appearance of preserved parathyroid glands after total thyroidectomy. Surg Today, 2016, 46(3): 356-362.
7. 周東懷, 張瑞廣, 廖斌, 等. 甲狀腺全切除術中對甲狀旁腺特異性附著脂肪進行保護的臨床和解剖分析. 中國醫藥科學, 2018, 8(6): 167-170.
8. Lang BHH, Chan DTY, Chow FCL, et al. The association of discolored parathyroid glands and hypoparathyroidism following total thyroidectomy. World J Surg, 2016, 40(7): 1611-1617.
9. Promberger R, Ott J, Kober F, et al. Normal parathyroid hormone levels do not exclude permanent hypoparathyroidism after thyroidectomy. Thyroid, 2011, 21(2): 145-150.
10. 郭飛躍, 耿勝杰, 張靜. 甲狀旁腺自體熒光顯像技術的研究進展. 臨床耳鼻咽喉頭頸外科雜志, 2022, 36(5): 397-401.
11. 宋西成, 鄭海濤. 甲狀旁腺自熒光顯影技術應用研究. 山東大學耳鼻喉眼學報, 2020, 34(3): 19-25.
12. 鄭偉慧, 王可敬. 甲狀腺手術中甲狀旁腺顯影的臨床應用進展. 腫瘤學雜志, 2022, 28(4): 327-331.
13. Landsman ML, Kwant G, Mook GA, et al. Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol, 1976, 40(4): 575-583.
14. Alander JT, Kaartinen I, Laakso A, et al. A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging, 2012, 2012: 940585. doi: 10.1155/2012/940585.
15. 吳國聰, 李俊, 徐威, 等. 吲哚菁綠顯像在預防腹腔鏡結直腸癌根治術后吻合口漏中的應用. 西部醫學, 2021, 33(7): 1035-1038.
16. 張寒, 游曉波, 蔡震, 等. 吲哚菁綠熒光造影技術在惡性黑色素瘤前哨淋巴結活檢中的應用探討. 實用醫院臨床雜志, 2020, 17(3): 231-232.
17. Kahramangil B, Berber E. The use of near-infrared fluorescence imaging in endocrine surgical procedures. J Surg Oncol, 2017, 115(7): 848-855.
18. 張珂, 趙輝, 時琳琳, 等. 吲哚菁綠熒光成像技術在甲狀旁腺和甲狀腺手術中的應用研究進展. 浙江醫學, 2021, 43(20): 2254-2257, 2262.
19. 任正君. 吲哚菁綠(ICG)熒光顯像在甲狀腺手術中保護甲狀旁腺和預測術后低鈣血癥的應用. 河北醫科大學, 2021. doi:10.27111/d.cnki.ghyku.2021.000731.
20. 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.
21. Lang B HH, Wong CKH, 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. 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.
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. Vidal Fortuny J, Guigard S, Diaper J, et al. Subtotal parathyroidectomy under indocyanine green angiography. VideoEndocrinology, 2016, 3(1): ve. 2015.0056. doi: 10.1089/ve.2015.0056.
25. 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.
26. Yavuz E, Biricik A, Karagulle OO, et al. A comparison of the quantitative evaluation of in situ parathyroid gland perfusion by indocyanine green fluorescence angiography and by visual examination in thyroid surgery. Arch Endocrinol Metab, 2020, 64(4): 427-435.
27. Priyanka S, Sam ST, Rebekah G, et al. The utility of indocyanine green (ICG) for the identification and assessment of viability of the parathyroid glands during thyroidectomy. Updates Surg, 2022, 74(1): 97-105.
28. Noltes ME, Metman MJH, Heeman W, et al. A novel and generic workflow of indocyanine green perfusion assessment integrating standardization and quantification toward clinical implementation. Ann Surg, 2021, 274(6): e659-e663. doi: 10.1097/SLA.0000000000004978.
29. Paras C, Keller M, White L, et al. Near-infrared autofluorescence for the detection of parathyroid glands. J Biomed Opt, 2011, 16(6): 067012. doi: 10.1117/1.3583571.
30. Di Marco AN, Palazzo FF. Near-infrared autofluorescence in thyroid and parathyroid surgery. Gland Surg, 2020, 9(Suppl 2): S136-S146. doi: 10.21037/gs.2020.01.04.
31. Shinden Y, Nakajo A, Arima H, et al. Intraoperative identification of the parathyroid gland with a fluorescence detection system. World J Surg, 2017, 41(6): 1506-1512.
32. De Leeuw F, Breuskin I, Abbaci M, et al. Intraoperative near-infrared imaging for parathyroid gland identification by auto-fluorescence: a feasibility study. World J Surg, 2016, 40(9): 2131-2138.
33. 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.
34. Jin H, Fan J, Yang J, et al. Application of indocyanine green in the parathyroid detection and protection: Report of 3 cases. Am J Otolaryngol, 2019, 40(2): 323-330.
35. Lerchenberger M, Al Arabi N, Gallwas JKS, et al. Intraoperative near-infrared autofluorescence and indocyanine green imaging to identify parathyroid glands: a comparison. Int J Endocrinol, 2019, 2019: 4687951. doi: 10.1155/2019/4687951.
36. Parfentiev R, Grubnik V, Grubnik V, et al. Study of intraoperative indocyanine green angiography effectiveness for identification of parathyroid gland during total thyroidectomy. Georgian medical news, 2021, 314: 26-29.
37. Oh E, Lee HC, Kim Y, et al. A pilot feasibility study to assess vascularity and perfusion of parathyroid glands using a portable hand-held imager. Lasers Surg Med, 2022, 54(3): 399-406.
38. Lo CY. Parathyroid autotransplantation during thyroidectomy. ANZ J Surg, 2002, 72(12): 902-907.
39. Aminfar A, Davoodzadeh N, Aguilar G, et al. Application of optical flow algorithms to laser speckle imaging. Microvasc Res, 2019, 122: 52-59.
40. Heeman W, Steenbergen W, van Dam G, et al. Clinical applications of laser speckle contrast imaging: a review. J Biomed Opt, 2019, 24(8): 1-11.
41. 李鵬程. 生物組織高分辨激光散斑血流成像技術研究. 第八屆全國光生物學學術會議論文摘要集. 2013, 24.
42. Boas DA, Dunn AK. Laser speckle contrast imaging in biomedical optics. J Biomed Opt, 2010, 15(1): 011109. doi: 10.1117/1.3285504.
43. To C, Rees-Lee JE, Gush RJ, et al. Intraoperative tissue perfusion measurement by laser speckle imaging: A potential aid for reducing postoperative complications in free flap breast reconstruction. Plast Reconstr Surg, 2019, 143(2): 287e-292e. doi: 10.1097/PRS.0000000000005223.
44. Mannoh EA, Thomas G, Solórzano CC, et al. Intraoperative assessment of parathyroid viability using laser speckle contrast imaging. Sci Rep, 2017, 7(1): 14798. doi: 10.1038/s41598-017-14941-5.
45. Mannoh EA, Thomas G, Baregamian N, et al. Assessing intraoperative laser speckle contrast imaging of parathyroid glands in relation to total thyroidectomy patient outcomes. Thyroid, 2021, 31(10): 1558-1565.
46. Mannoh EA, Parker LB, Thomas G, et al. Development of an imaging device for label-free parathyroid gland identification and vascularity assessment. J Biophotonics, 2021, 14(6): e202100008. doi: 10.1002/jbio.202100008.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Progress of fluorescence imaging in the study of parathyroid blood supply

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