Progress of autofluorescence in the study of parathyroid gland_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

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

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

Corresponding author：

ZHENG Haitao, Email: zhenghaitao1972@126.com

Keywords：

thyroid; parathyroid gland; near-infrared autofluorescence imaging

DOI：

10.7507/1007-9424.202208043

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the development, clinical application, advantages and disadvantages, and future prospects of parathyroid autofluorescence in recent years. Method The literatures related to the research progress of parathyroid autofluorescence in recent years were searched, and launched a specific discussion. Results Autofluorescence of parathyroid gland was still in its infancy at home and abroad. The existing studies had shown that this technique was superior to visual recognition and could reduce the incidence of postoperative complications. Autofluorescence technology had shown some advantages in identifying parathyroid gland during operation, and its mechanism research and related equipment improvement should be focused in the future. Conclusion Autofluorescence technique is of great value in the identification of parathyroid glands in patients undergoing thyroidectomy or parathyroidectomy.

Citation： YANG Xiaoqing, WANG Zhengzhai, LIN Xiyuan, ZHENG Haitao. Progress of autofluorescence in the study of parathyroid gland. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(2): 236-241. doi: 10.7507/1007-9424.202208043 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.	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.
3.	Bergamaschi R, Becouarn G, Ronceray J, et al. Morbidity of thyroid surgery. Am J Surg, 1998, 176(1): 71-75.
4.	Ladurner R, Al Arabi N, Guendogar U, et al. Near-infrared autofluorescence imaging to detect parathyroid glands in thyroid surgery. Ann R Coll Surg Engl, 2018, 100(1): 33-36.
5.	Das K, Stone N, Kendall C, et al. Raman spectroscopy of parathyroid tissue pathology. Lasers Med Sci, 2006, 21(4): 192-197.
6.	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.
7.	McWade MA, Paras C, White LM, et al. A novel optical approach to intraoperative detection of parathyroid glands. Surgery, 2013, 154(6): 1371-1377.
8.	Hyun H, Park MH, Owens EA, et al. Structure-inherent targeting of near-infrared fluorophores for parathyroid and thyroid gland imaging. Nat Med, 2015, 21(2): 192-197.
9.	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.
10.	Berber E, Akbulut S. Can near-infrared autofluorescence imaging be used for intraoperative confirmation of parathyroid tissue? J Surg Oncol, 2021, 124(7): 1008-1013.
11.	Kim DH, Lee S, Jung J, et al. Near-infrared autofluorescence-based parathyroid glands identification in the thyroidectomy or parathyroidectomy: a systematic review and meta-analysis. Langenbecks Arch Surg, 2022, 407(2): 491-499.
12.	Kiernan CM, Thomas G, Baregamian N, et al. Initial clinical experiences using the intraoperative probe-based parathyroid autofluorescence identification system-PTeye^TM during thyroid and parathyroid procedures. J Surg Oncol, 2021, 124(3): 271-281.
13.	Thomas G, Mcwade MA, Nguyen JQ, et al. Innovative surgical guidance for label-free real-time parathyroid identification. Surgery, 2019, 165(1): 114-123.
14.	Ladurner R, Al Arabi N, Guendogar U, et al. Near-infrared autofluorescence imaging to detect parathyroid glands in thyroid surgery. Ann R Coll Surg Engl, 2018, 100(1): 33-36.
15.	Rodriguez M, Nemeth E, Martin D. The calcium-sensing receptor: a key factor in the pathogenesis of secondary hyperparathyroidism. Am J Physiol Renal Physiol, 2005, 288(2): F253-F264.
16.	McWade MA, Paras C, White LM, et al. Label-free intraoperative parathyroid localization with near-infrared autofluorescence imaging. J Clin Endocrinol Metab, 2014, 99(12): 4574-4580.
17.	McWade MA, Sanders ME, Broome JT, et al. Establishing the clinical utility of autofluorescence spectroscopy for parathyroid detection. Surgery, 2016, 159(1): 193-203.
18.	Ladurner R, Sommerey S, Arabi NA, et al. Intraoperative near-infrared autofluorescence imaging of parathyroid glands. Surg Endosc, 2017, 31(8): 3140-3145.
19.	Falco J, Dip F, Quadri P, et al. Cutting edge in thyroid surgery: autofluorescence of parathyroid glands. J Am Coll Surg, 2016, 223(2): 374-380.
20.	Demarchi MS, Karenovics W, Bedat B, et al. Autofluorescence pattern of parathyroid adenomas. BJS Open, 2021, 5(1): zraa047. doi:10.1093/bjsopen/zraa047.
21.	Law RH, Larrabee KA, Van Harn M, et al. Parathyroid gland autofluorescence characteristics in patients with primary hyperparathyroidism. Laryngoscope, 2022, 132(3): 715-721.
22.	Kose E, Kahramangil B, Aydin H, et al. Heterogeneous and low-intensity parathyroid autofluorescence: patterns suggesting hyperfunction at parathyroid exploration. Surgery, 2019, 165(2): 431-437.
23.	Kahramangil B, Berber E. The use of near-infrared fluorescence imaging in endocrine surgical procedures. J Surg Oncol, 2017, 115(7): 848-855.
24.	Falco J, Dip F, Quadri P, et al. Increased identification of parathyroid glands using near infrared light during thyroid and parathyroid surgery. Surg Endosc, 2017, 31(9): 3737-3742.
25.	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.
26.	Serra C, Silveira L, Canudo A, et al. Parathyroid identification by autofluorescence— preliminary report on five cases of surgery for primary hyperparathyroidism. BMC Surg, 2019, 19(1): 120. doi:10.1186/s12893-019-0590-9.
27.	Squires MH, Jarvis R, Shirley LA, et al. Intraoperative parathyroid autofluorescence detection in patients with primary hyperparathyroidism. Ann Surg Oncol, 2019, 26(4): 1142-1148.
28.	王涛, 柳桢, 张朋宇, 等. 近红外荧光下甲状旁腺自体荧光强度潜在影响因素分析及其对术中甲状旁腺识别的指导. 中华耳鼻咽喉头颈外科杂志, 2020, 55(5): 490-496.
29.	Kim SW, Song SH, Lee HS, et al. Intraoperative real-time localization of normal parathyroid glands with autofluorescence imaging. J Clin Endocrinol Metab, 2016, 101(12): 4646-4652.
30.	Hu Y, Han AY, Huang S, et al. A tool to locate parathyroid glands using dynamic optical contrast imaging. Laryngoscope, 2021, 131(10): 2391-2397.
31.	Kose E, Rudin AV, Kahramangil B, et al. Autofluorescence imaging of parathyroid glands: an assessment of potential indications. Surgery, 2020, 167(1): 173-178.
32.	Kahramangil B, Dip F, Benmiloud F, et al. Detection of parathyroid autofluorescence using near-infrared imaging: a multicenter analysis of concordance between different surgeons. Ann Surg Oncol, 2018, 25(4): 957-962.
33.	Benmiloud F, Rebaudet S, Varoquaux A, et al. Impact of autofluorescence-based identification of parathyroids during total thyroidectomy on postoperative hypocalcemia: a before and after controlled study. Surgery, 2018, 163(1): 23-29.
34.	Dip F, Falco J, Verna S, et al. Randomized controlled trial comparing white light with near-infrared autofluorescence for parathyroid gland identification during total thyroidectomy. J Am Coll Surg, 2019, 228(5): 744-751.
35.	Kim SW, Lee HS, Ahn YC, et al. Near-infrared autofluorescence image-guided parathyroid gland mapping in thyroidectomy. J Am Coll Surg, 2018, 226(2): 165-172.
36.	Wolf HW, Grumbeck B, Runkel N. Intraoperative verification of parathyroid glands in primary and secondary hyperparathyroidism using near-infrared autofluorescence (IOPA). Updates Surg, 2019, 71(3): 579-585.
37.	Kikumori T, Inaishi T, Miyajima N, et al. Robust, quick, and convenient intraoperative method to differentiate parathyroid tissue. Surgery, 2020, 167(2): 385-389.
38.	Benmiloud F, Godiris-Petit G, Gras R, et al. Association of autofluorescence-based detection of the parathyroid glands during total thyroidectomy with postoperative hypocalcemia risk results of the PARAFLUO multicenter randomized clinical trial. JAMA Surg, 2020, 155(2): 106-112.
39.	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.
40.	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.
41.	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.
42.	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.
43.	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.
44.	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.
45.	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. 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.
3. Bergamaschi R, Becouarn G, Ronceray J, et al. Morbidity of thyroid surgery. Am J Surg, 1998, 176(1): 71-75.
4. Ladurner R, Al Arabi N, Guendogar U, et al. Near-infrared autofluorescence imaging to detect parathyroid glands in thyroid surgery. Ann R Coll Surg Engl, 2018, 100(1): 33-36.
5. Das K, Stone N, Kendall C, et al. Raman spectroscopy of parathyroid tissue pathology. Lasers Med Sci, 2006, 21(4): 192-197.
6. 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.
7. McWade MA, Paras C, White LM, et al. A novel optical approach to intraoperative detection of parathyroid glands. Surgery, 2013, 154(6): 1371-1377.
8. Hyun H, Park MH, Owens EA, et al. Structure-inherent targeting of near-infrared fluorophores for parathyroid and thyroid gland imaging. Nat Med, 2015, 21(2): 192-197.
9. 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.
10. Berber E, Akbulut S. Can near-infrared autofluorescence imaging be used for intraoperative confirmation of parathyroid tissue? J Surg Oncol, 2021, 124(7): 1008-1013.
11. Kim DH, Lee S, Jung J, et al. Near-infrared autofluorescence-based parathyroid glands identification in the thyroidectomy or parathyroidectomy: a systematic review and meta-analysis. Langenbecks Arch Surg, 2022, 407(2): 491-499.
12. Kiernan CM, Thomas G, Baregamian N, et al. Initial clinical experiences using the intraoperative probe-based parathyroid autofluorescence identification system-PTeye^TM during thyroid and parathyroid procedures. J Surg Oncol, 2021, 124(3): 271-281.
13. Thomas G, Mcwade MA, Nguyen JQ, et al. Innovative surgical guidance for label-free real-time parathyroid identification. Surgery, 2019, 165(1): 114-123.
14. Ladurner R, Al Arabi N, Guendogar U, et al. Near-infrared autofluorescence imaging to detect parathyroid glands in thyroid surgery. Ann R Coll Surg Engl, 2018, 100(1): 33-36.
15. Rodriguez M, Nemeth E, Martin D. The calcium-sensing receptor: a key factor in the pathogenesis of secondary hyperparathyroidism. Am J Physiol Renal Physiol, 2005, 288(2): F253-F264.
16. McWade MA, Paras C, White LM, et al. Label-free intraoperative parathyroid localization with near-infrared autofluorescence imaging. J Clin Endocrinol Metab, 2014, 99(12): 4574-4580.
17. McWade MA, Sanders ME, Broome JT, et al. Establishing the clinical utility of autofluorescence spectroscopy for parathyroid detection. Surgery, 2016, 159(1): 193-203.
18. Ladurner R, Sommerey S, Arabi NA, et al. Intraoperative near-infrared autofluorescence imaging of parathyroid glands. Surg Endosc, 2017, 31(8): 3140-3145.
19. Falco J, Dip F, Quadri P, et al. Cutting edge in thyroid surgery: autofluorescence of parathyroid glands. J Am Coll Surg, 2016, 223(2): 374-380.
20. Demarchi MS, Karenovics W, Bedat B, et al. Autofluorescence pattern of parathyroid adenomas. BJS Open, 2021, 5(1): zraa047. doi:10.1093/bjsopen/zraa047.
21. Law RH, Larrabee KA, Van Harn M, et al. Parathyroid gland autofluorescence characteristics in patients with primary hyperparathyroidism. Laryngoscope, 2022, 132(3): 715-721.
22. Kose E, Kahramangil B, Aydin H, et al. Heterogeneous and low-intensity parathyroid autofluorescence: patterns suggesting hyperfunction at parathyroid exploration. Surgery, 2019, 165(2): 431-437.
23. Kahramangil B, Berber E. The use of near-infrared fluorescence imaging in endocrine surgical procedures. J Surg Oncol, 2017, 115(7): 848-855.
24. Falco J, Dip F, Quadri P, et al. Increased identification of parathyroid glands using near infrared light during thyroid and parathyroid surgery. Surg Endosc, 2017, 31(9): 3737-3742.
25. 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.
26. Serra C, Silveira L, Canudo A, et al. Parathyroid identification by autofluorescence— preliminary report on five cases of surgery for primary hyperparathyroidism. BMC Surg, 2019, 19(1): 120. doi:10.1186/s12893-019-0590-9.
27. Squires MH, Jarvis R, Shirley LA, et al. Intraoperative parathyroid autofluorescence detection in patients with primary hyperparathyroidism. Ann Surg Oncol, 2019, 26(4): 1142-1148.
28. 王涛, 柳桢, 张朋宇, 等. 近红外荧光下甲状旁腺自体荧光强度潜在影响因素分析及其对术中甲状旁腺识别的指导. 中华耳鼻咽喉头颈外科杂志, 2020, 55(5): 490-496.
29. Kim SW, Song SH, Lee HS, et al. Intraoperative real-time localization of normal parathyroid glands with autofluorescence imaging. J Clin Endocrinol Metab, 2016, 101(12): 4646-4652.
30. Hu Y, Han AY, Huang S, et al. A tool to locate parathyroid glands using dynamic optical contrast imaging. Laryngoscope, 2021, 131(10): 2391-2397.
31. Kose E, Rudin AV, Kahramangil B, et al. Autofluorescence imaging of parathyroid glands: an assessment of potential indications. Surgery, 2020, 167(1): 173-178.
32. Kahramangil B, Dip F, Benmiloud F, et al. Detection of parathyroid autofluorescence using near-infrared imaging: a multicenter analysis of concordance between different surgeons. Ann Surg Oncol, 2018, 25(4): 957-962.
33. Benmiloud F, Rebaudet S, Varoquaux A, et al. Impact of autofluorescence-based identification of parathyroids during total thyroidectomy on postoperative hypocalcemia: a before and after controlled study. Surgery, 2018, 163(1): 23-29.
34. Dip F, Falco J, Verna S, et al. Randomized controlled trial comparing white light with near-infrared autofluorescence for parathyroid gland identification during total thyroidectomy. J Am Coll Surg, 2019, 228(5): 744-751.
35. Kim SW, Lee HS, Ahn YC, et al. Near-infrared autofluorescence image-guided parathyroid gland mapping in thyroidectomy. J Am Coll Surg, 2018, 226(2): 165-172.
36. Wolf HW, Grumbeck B, Runkel N. Intraoperative verification of parathyroid glands in primary and secondary hyperparathyroidism using near-infrared autofluorescence (IOPA). Updates Surg, 2019, 71(3): 579-585.
37. Kikumori T, Inaishi T, Miyajima N, et al. Robust, quick, and convenient intraoperative method to differentiate parathyroid tissue. Surgery, 2020, 167(2): 385-389.
38. Benmiloud F, Godiris-Petit G, Gras R, et al. Association of autofluorescence-based detection of the parathyroid glands during total thyroidectomy with postoperative hypocalcemia risk results of the PARAFLUO multicenter randomized clinical trial. JAMA Surg, 2020, 155(2): 106-112.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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 autofluorescence in the study of parathyroid gland

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