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.	郑荣寿, 孙可欣, 张思维, 等. 2015年中国恶性肿瘤流行情况分析. 中华肿瘤杂志, 2019, 41(1): 19-28.
2.	中国医师协会外科医师分会甲状腺外科医师委员会. 甲状腺手术中甲状旁腺保护专家共识. 中国实用外科杂志, 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, 贺晨宇, 贺建业, 等. 小切口腔镜辅助甲状腺手术中不同张力操作对上位甲状旁腺血运的影响. 中国微创外科杂志, 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.	周东怀, 张瑞广, 廖斌, 等. 甲状腺全切除术中对甲状旁腺特异性附着脂肪进行保护的临床和解剖分析. 中国医药科学, 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.	郭飞跃, 耿胜杰, 张静. 甲状旁腺自体荧光显像技术的研究进展. 临床耳鼻咽喉头颈外科杂志, 2022, 36(5): 397-401.
11.	宋西成, 郑海涛. 甲状旁腺自荧光显影技术应用研究. 山东大学耳鼻喉眼学报, 2020, 34(3): 19-25.
12.	郑伟慧, 王可敬. 甲状腺手术中甲状旁腺显影的临床应用进展. 肿瘤学杂志, 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.	吴国聪, 李俊, 徐威, 等. 吲哚菁绿显像在预防腹腔镜结直肠癌根治术后吻合口漏中的应用. 西部医学, 2021, 33(7): 1035-1038.
16.	张寒, 游晓波, 蔡震, 等. 吲哚菁绿荧光造影技术在恶性黑色素瘤前哨淋巴结活检中的应用探讨. 实用医院临床杂志, 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.	张珂, 赵辉, 时琳琳, 等. 吲哚菁绿荧光成像技术在甲状旁腺和甲状腺手术中的应用研究进展. 浙江医学, 2021, 43(20): 2254-2257, 2262.
19.	任正君. 吲哚菁绿(ICG)荧光显像在甲状腺手术中保护甲状旁腺和预测术后低钙血症的应用. 河北医科大学, 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.	李鹏程. 生物组织高分辨激光散斑血流成像技术研究. 第八届全国光生物学学术会议论文摘要集. 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. 郑荣寿, 孙可欣, 张思维, 等. 2015年中国恶性肿瘤流行情况分析. 中华肿瘤杂志, 2019, 41(1): 19-28.
2. 中国医师协会外科医师分会甲状腺外科医师委员会. 甲状腺手术中甲状旁腺保护专家共识. 中国实用外科杂志, 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, 贺晨宇, 贺建业, 等. 小切口腔镜辅助甲状腺手术中不同张力操作对上位甲状旁腺血运的影响. 中国微创外科杂志, 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. 周东怀, 张瑞广, 廖斌, 等. 甲状腺全切除术中对甲状旁腺特异性附着脂肪进行保护的临床和解剖分析. 中国医药科学, 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. 郭飞跃, 耿胜杰, 张静. 甲状旁腺自体荧光显像技术的研究进展. 临床耳鼻咽喉头颈外科杂志, 2022, 36(5): 397-401.
11. 宋西成, 郑海涛. 甲状旁腺自荧光显影技术应用研究. 山东大学耳鼻喉眼学报, 2020, 34(3): 19-25.
12. 郑伟慧, 王可敬. 甲状腺手术中甲状旁腺显影的临床应用进展. 肿瘤学杂志, 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. 吴国聪, 李俊, 徐威, 等. 吲哚菁绿显像在预防腹腔镜结直肠癌根治术后吻合口漏中的应用. 西部医学, 2021, 33(7): 1035-1038.
16. 张寒, 游晓波, 蔡震, 等. 吲哚菁绿荧光造影技术在恶性黑色素瘤前哨淋巴结活检中的应用探讨. 实用医院临床杂志, 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. 张珂, 赵辉, 时琳琳, 等. 吲哚菁绿荧光成像技术在甲状旁腺和甲状腺手术中的应用研究进展. 浙江医学, 2021, 43(20): 2254-2257, 2262.
19. 任正君. 吲哚菁绿(ICG)荧光显像在甲状腺手术中保护甲状旁腺和预测术后低钙血症的应用. 河北医科大学, 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. 李鹏程. 生物组织高分辨激光散斑血流成像技术研究. 第八届全国光生物学学术会议论文摘要集. 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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