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Role of Indocyanine Green in Breast Surgery

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Abstract

The objective of this paper is to give a synopsis of the recent surgical applications of indocyanine green fluorescence imaging methods in breast and breast-related surgeries; the basics of the technology and instrumentation used. Well over 200 papers describing this technique in clinical settings were reviewed. In addition to the surgical applications, other recent medical applications of ICG in breast surgeries are briefly examined. There is currently enough evidence suggesting that reverse lymphatic mapping and SLNB using ICG lymphography provide similar results to those using technetium-99 isotope scanning (Pons et al. Plast Reconstr Surg 147(2):207e–12e, 2021). Postoperative mastectomy skin flap necrosis could be thwarted by using intraoperative ICGA to identify mastectomy skin flap areas of inadequate perfusion. It is also one of the most objective and reliable methods to directly assess tissue perfusion in free flap reconstructive surgery, and result in an improvement of (partial) flap survival. Fluorescence imaging is a minimally invasive imaging modality that is useful for the preoperative detection of lymphatic vessels by mapping linear patterns on the patient’s limb and useful in both lymphaticovenular anastomosis and lymphedema screening.

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References

  1. Alander JT, Kaartinen I, Laakso A, Pätilä T, Spillmann T, Tuchin VV et al (2012) A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging. 2012:e940585

    Article  Google Scholar 

  2. Choi M, Choi K, Ryu S-W, Lee J, Choi C (2011) Dynamic fluorescence imaging for multiparametric measurement of tumor vasculature. J Biomed Opt. 16(4):046008

    Article  PubMed  Google Scholar 

  3. Liu Y, Bauer AQ, Akers WJ, Sudlow G, Liang K, Shen D et al (2011) Hands-free, wireless goggles for near-infrared fluorescence and real-time image-guided surgery. Surgery 149(5):689–698

    Article  PubMed  Google Scholar 

  4. Lee BT, Matsui A, Hutteman M, Lin SJ, Winer JH, Laurence RG et al (2010) Intraoperative near-infrared fluorescence imaging in perforator flap reconstruction: current research and early clinical experience. J Reconstr Microsurg 26(1):59–65

    Article  PubMed  Google Scholar 

  5. Foster D, Choy N, Porter C, Ahmed S, Wapnir I (2018) Axillary reverse mapping with indocyanine green or isosulfan blue demonstrate similar crossover rates to radiotracer identified sentinel nodes. J Surg Oncol 117(3):336–340

    Article  CAS  PubMed  Google Scholar 

  6. Wu J-D, Wang Z, Zeng H-C, He L-F, Zhang Y-Q, Huang G-S et al (2020) Comparison of indocyanine green and methylene blue use for axillary reverse mapping during axillary lymph node dissection. MedComm 1(2):211–218

    Article  PubMed  PubMed Central  Google Scholar 

  7. Zhang X, Li Y, Zhou Y, Mao F, Lin Y, Guan J et al (2016) Diagnostic performance of indocyanine green-guided sentinel lymph node biopsy in breast cancer: a meta-analysis. PLoS ONE. 11(6):e0155597

    Article  PubMed  PubMed Central  Google Scholar 

  8. Vermersch C, Raia-Barjat T, Chapelle C, Lima S, Chauleur C (2019) Randomized comparison between indocyanine green fluorescence plus 99mtechnetium and 99mtechnetium alone methods for sentinel lymph node biopsy in breast cancer. Sci Rep 9:6943

    Article  PubMed  PubMed Central  Google Scholar 

  9. Wishart GC, Loh S-W, Jones L, Benson JR (2012) A feasibility study (ICG-10) of indocyanine green (ICG) fluorescence mapping for sentinel lymph node detection in early breast cancer. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 38(8):651–656

    CAS  Google Scholar 

  10. Jeremiasse B, van den Bosch CH, Wijnen MWHA, Terwisscha van Scheltinga CEJ, Fiocco MF, van der Steeg AFW (2020) Systematic review and meta-analysis concerning near-infrared imaging with fluorescent agents to identify the sentinel lymph node in oncology patients. Eur J Surg Oncol. 46(11):2011–22

    Article  CAS  PubMed  Google Scholar 

  11. Subcutaneous mastectomy. A review of 130 cases—PubMed. [cited 2021 Aug 23]. Available from: https://pubmed.ncbi.nlm.nih.gov/3397255/

  12. Boneti C, Yuen J, Santiago C, Diaz Z, Robertson Y, Korourian S et al (2011) Oncologic safety of nipple skin-sparing or total skin-sparing mastectomies with immediate reconstruction. J Am Coll Surg. 212(4):686–93; discussion 693-695

    Article  PubMed  Google Scholar 

  13. Kissin MW, Kark AE (1987) Nipple preservation during mastectomy. Br J Surg 74(1):58–61

    Article  CAS  PubMed  Google Scholar 

  14. Carlson GW (1996) Skin sparing mastectomy: anatomic and technical considerations. Am Surg 62(2):151–155

    CAS  PubMed  Google Scholar 

  15. Garwood ER, Moore D, Ewing C, Hwang ES, Alvarado M, Foster RD et al (2009) Total skin-sparing mastectomy: complications and local recurrence rates in 2 cohorts of patients. Ann Surg 249(1):26–32

    Article  PubMed  Google Scholar 

  16. Phillips BT, Lanier ST, Conkling N, Wang ED, Dagum AB, Ganz JC et al (2012) Intraoperative perfusion techniques can accurately predict mastectomy skin flap necrosis in breast reconstruction: results of a prospective trial. Plast Reconstr Surg 129(5):778e-e788

    Article  PubMed  Google Scholar 

  17. Holm C, Mayr M, Höfter E, Becker A, Pfeiffer UJ, Mühlbauer W (2002) Intraoperative evaluation of skin-flap viability using laser-induced fluorescence of indocyanine green. Br J Plast Surg 55(8):635–644

    Article  CAS  PubMed  Google Scholar 

  18. Newman MI, Samson MC (2009) The application of laser-assisted indocyanine green fluorescent dye angiography in microsurgical breast reconstruction. J Reconstr Microsurg 25(1):21–26

    Article  PubMed  Google Scholar 

  19. Newman MI, Samson MC, Tamburrino JF, Swartz KA (2010) Intraoperative laser-assisted indocyanine green angiography for the evaluation of mastectomy flaps in immediate breast reconstruction. J Reconstr Microsurg 26(7):487–492

    Article  PubMed  Google Scholar 

  20. Pestana IA, Coan B, Erdmann D, Marcus J, Levin LS, Zenn MR (2009) Early experience with fluorescent angiography in free-tissue transfer reconstruction. Plast Reconstr Surg 123(4):1239–1244

    Article  CAS  PubMed  Google Scholar 

  21. Lauritzen E, Damsgaard TE (2021) Use of indocyanine green angiography decreases the risk of complications in autologous- and implant-based breast reconstruction: a systematic review and meta-analysis. J Plast Reconstr Aesthet Surg 74(8):1703–1717

    Article  PubMed  Google Scholar 

  22. Pruimboom T, Schols RM, Van Kuijk SM, Van der Hulst RR, Qiu SS (2019) Indocyanine green angiography for preventing postoperative mastectomy skin flap necrosis in immediate breast reconstruction. Cochrane Breast Cancer Group, editor. Cochrane Database Syst Rev. [cited 2021 Aug 25]; Available from: https://doi.wiley.com/10.1002/14651858.CD013280

  23. McIvor NP (1993) How to manage the failed free flap. Oper Tech Otolaryngol-Head Neck Surg 4(2):165–168

    Article  Google Scholar 

  24. Liu DZ, Mathes DW, Zenn MR, Neligan PC (2011) The application of indocyanine green fluorescence angiography in plastic surgery. J Reconstr Microsurg 27(6):355–364

    Article  CAS  PubMed  Google Scholar 

  25. Chae MP, Rozen WM, Whitaker IS, Chubb D, Grinsell D, Ashton MW et al (2015) Current evidence for postoperative monitoring of microvascular free flaps: a systematic review. Ann Plast Surg 74(5):621–632

    Article  CAS  PubMed  Google Scholar 

  26. Jakubietz RG, Schmidt K, Bernuth S, Meffert RH, Jakubietz MG (2019) Evaluation of the intraoperative blood flow of pedicled perforator flaps using indocyanine green-fluorescence angiography. Plast Reconstr Surg Glob Open. 7(9):e2462

    PubMed  PubMed Central  Google Scholar 

  27. Smit JM, Negenborn VL, Jansen SM, Jaspers MEH, de Vries R, Heymans MW et al (2018) Intraoperative evaluation of perfusion in free flap surgery: a systematic review and meta-analysis. Microsurgery 38(7):804–818

    Article  PubMed  Google Scholar 

  28. Koshima I, Narushima M, Mihara M, Yamamoto T, Hara H, Ohshima A et al (2016) Lymphadiposal flaps and lymphaticovenular anastomoses for severe leg edema: functional reconstruction for lymph drainage system. J Reconstr Microsurg 32(1):50–55

    PubMed  Google Scholar 

  29. Yamamoto T, Iida T, Yoshimatsu H, Fuse Y, Hayashi A, Yamamoto N (2018) Lymph flow restoration after tissue replantation and transfer: importance of lymph axiality and possibility of lymph flow reconstruction without lymph node transfer or lymphatic anastomosis. Plast Reconstr Surg 142(3):796–804

    Article  CAS  PubMed  Google Scholar 

  30. Hong JP, Choi DH, Suh H, Mukarramah DA, Tashti T, Lee K et al (2014) A new plane of elevation: the superficial fascial plane for perforator flap elevation. J Reconstr Microsurg 30(7):491–496

    Article  PubMed  Google Scholar 

  31. Kim JH, Kim KN, Yoon CS (2015) Reconstruction of moderate-sized distal limb defects using a superthin superficial circumflex iliac artery perforator flap. J Reconstr Microsurg 31(9):631–635

    Article  PubMed  Google Scholar 

  32. Feng S, Xi W, Zhang Z, Tremp M, Schaefer DJ, Sadigh PL et al (2017) A reappraisal of the surgical planning of the superficial circumflex iliac artery perforator flap. J Plast Reconstr Aesthetic Surg JPRAS 70(4):469–477

    Article  PubMed  Google Scholar 

  33. Schacht V, Luedemann W, Abels C, Berens von Rautenfeld D (2009) Anatomy of the subcutaneous lymph vascular network of the human leg in relation to the great saphenous vein. Anat Rec Hoboken NJ 292(1):87–93

    Article  Google Scholar 

  34. Yamada Y (1969) The studies on lymphatic venous anastomosis in lvmphedema. Nagoya J Med Sci 32(1):1–21

    Google Scholar 

  35. O’Brien BM, Sykes P, Threlfall GN, Browning FS (1977) Microlymphaticovenous anastomoses for obstructive lymphedema. Plast Reconstr Surg 60(2):197–211

    Article  PubMed  Google Scholar 

  36. Yamamoto T, Narushima M, Yoshimatsu H, Seki Y, Yamamoto N, Oka A et al (2014) Minimally invasive lymphatic supermicrosurgery (MILS): indocyanine green lymphography-guided simultaneous multisite lymphaticovenular anastomoses via millimeter skin incisions. Ann Plast Surg 72(1):67–70

    Article  CAS  PubMed  Google Scholar 

  37. Yang JC S, Wu S C, Chiang M-H, Lin W-C (2018) Targeting reflux-free veins with a vein visualizer to identify the ideal recipient vein preoperatively for optimal lymphaticovenous anastomosis in treating lymphedema. Plast Reconstr Surg. 141(3):793–7

    Article  CAS  PubMed  Google Scholar 

  38. Hayashi A, Hayashi N, Yoshimatsu H, Yamamoto T (2018) Effective and efficient lymphaticovenular anastomosis using preoperative ultrasound detection technique of lymphatic vessels in lower extremity lymphedema. J Surg Oncol 117(2):290–298

    Article  PubMed  Google Scholar 

  39. Chang DW, Masia J, Garza R, Skoracki R, Neligan PC (2016) Lymphedema: surgical and medical therapy. Plast Reconstr Surg 138(3 Suppl):209S-218S

    Article  CAS  PubMed  Google Scholar 

  40. Yamamoto T, Yamamoto N, Yoshimatsu H, Narushima M, Koshima I (2017) Factors associated with lymphosclerosis: an analysis on 962 lymphatic vessels. Plast Reconstr Surg 140(4):734–741

    Article  CAS  PubMed  Google Scholar 

  41. Akita S, Mitsukawa N, Rikihisa N, Kubota Y, Omori N, Mitsuhashi A et al (2013) Early diagnosis and risk factors for lymphedema following lymph node dissection for gynecologic cancer. Plast Reconstr Surg 131(2):283–290

    Article  CAS  PubMed  Google Scholar 

  42. Akita S, Nakamura R, Yamamoto N, Tokumoto H, Ishigaki T, Yamaji Y et al (2016) Early detection of lymphatic disorder and treatment for lymphedema following breast cancer. Plast Reconstr Surg 138(2):192e–202e

    Article  CAS  PubMed  Google Scholar 

  43. Ogata F, Narushima M, Mihara M, Azuma R, Morimoto Y, Koshima I (2007) Intraoperative lymphography using indocyanine green dye for near-infrared fluorescence labeling in lymphedema. Ann Plast Surg 59(2):180–184

    Article  CAS  PubMed  Google Scholar 

  44. Lymphedema Risk Factors (2016) Breastcancer.org. [cited 2021 Aug 30]. Available from: https://www.breastcancer.org/treatment/lymphedema/risk_factors

  45. Giacalone G, Yamamoto T, Hayashi A, Belva F, Gysen M, Hayashi N et al (2019) Lymphatic supermicrosurgery for the treatment of recurrent lymphocele and severe lymphorrhea. Microsurgery 39(4):326–331

    Article  PubMed  Google Scholar 

  46. Duewell S, Hagspiel KD, Zuber J, von Schulthess GK, Bollinger A, Fuchs WA (1992) Swollen lower extremity: role of MR imaging. Radiology 184(1):227–231

    Article  CAS  PubMed  Google Scholar 

  47. Tomczak H, Nyka W, Lass P (2005) Lymphoedema: lymphoscintigraphy versus other diagnostic techniques—a clinician’s point of view. Nucl Med Rev Cent East Eur 8(1):37–43

    PubMed  Google Scholar 

  48. Marotel M, Cluzan R, Ghabboun S, Pascot M, Alliot F, Lasry JL (1998) Transaxial computer tomography of lower extremity lymphedema. Lymphology 31(4):180–185

    CAS  PubMed  Google Scholar 

  49. Chang L, Cheng M-F, Chang H-H, Kao YH, Wu Y-W (2011) The role of lymphoscintigraphy in diagnosis and monitor the response of physiotherapeutic technique in congenital lymphedema. Clin Nucl Med 36(4):e11-12

    Article  PubMed  Google Scholar 

  50. Sadeghi R, Kazemzadeh G, Keshtgar M (2010) Diagnostic application of lymphoscintigraphy in the management of lymphoedema. Hell J Nucl Med 13(1):6–10

    PubMed  Google Scholar 

  51. Yamamoto T, Matsuda N, Doi K, Oshima A, Yoshimatsu H, Todokoro T et al (2011) The earliest finding of indocyanine green lymphography in asymptomatic limbs of lower extremity lymphedema patients secondary to cancer treatment: the modified dermal backflow stage and concept of subclinical lymphedema. Plast Reconstr Surg 128(4):314e-e321

    Article  CAS  PubMed  Google Scholar 

  52. Yamamoto T, Narushima M, Doi K, Oshima A, Ogata F, Mihara M et al (2011) Characteristic indocyanine green lymphography findings in lower extremity lymphedema: the generation of a novel lymphedema severity staging system using dermal backflow patterns. Plast Reconstr Surg 127(5):1979–1986

    Article  CAS  PubMed  Google Scholar 

  53. Yamamoto T, Matsuda N, Todokoro T, Yoshimatsu H, Narushima M, Mihara M et al (2011) Lower extremity lymphedema index: a simple method for severity evaluation of lower extremity lymphedema. Ann Plast Surg 67(6):637–640

    Article  CAS  PubMed  Google Scholar 

  54. Mihara M, Hara H, Araki J, Kikuchi K, Narushima M, Yamamoto T et al (2012) Indocyanine green (ICG) lymphography is superior to lymphoscintigraphy for diagnostic imaging of early lymphedema of the upper limbs. PLoS ONE 7(6):e381842

    Article  Google Scholar 

  55. Keller E, Wolf M, Martin M, Yonekawa Y (2001) Estimation of cerebral oxygenation and hemodynamics in cerebral vasospasm using indocyaningreen dye dilution and near infrared spectroscopy: a case report. J Neurosurg Anesthesiol 13(1):43–48

    Article  CAS  PubMed  Google Scholar 

  56. Predicting mastectomy skin flap necrosis with indocyanine green angiography: the gray area defined—PubMed. [cited 2021 Sep 2]. Available from: https://pubmed.ncbi.nlm.nih.gov/22544087/

  57. Schuette AJ, Dannenbaum MJ, Cawley CM, Barrow DL (2011) Indocyanine green videoangiography for confirmation of bypass graft patency. J Korean Neurosurg Soc 50(1):23–29

    Article  PubMed  PubMed Central  Google Scholar 

  58. Cavallo C, Gandhi S, Zhao X, Belykh E, Valli D, Nakaji P et al (2019) Applications of microscope-integrated indocyanine green videoangiography in cerebral revascularization procedures. Front Surg 6:59

    Article  PubMed  PubMed Central  Google Scholar 

  59. Matsumoto H, Yoshida Y (2018) Usefulness of intraoperative indocyanine green video angiography to select the recipient artery for bypass surgery in arteriosclerotic occlusion of the middle cerebral artery: a technical case report. Chin Neurosurg J 4(1):20

    Article  PubMed  PubMed Central  Google Scholar 

  60. Pons G, Abdelfattah U, Sarria J, Duch J, Masia J (2021) Reverse lymph node mapping using indocyanine green lymphography: a step forward in minimizing donor-site morbidity in vascularized lymph node transfer. Plast Reconstr Surg 147(2):207e-e212

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Plastic, Cosmetic, and Reconstructive Surgery, Manipal Hospital, Bangalore, India

    Ashok B. C., Harish Kumar Kabilan, Anantheswar Y. N. & Srikanth V.

  2. Department of Surgical Oncology, Manipal Comprehensive Cancer Centre, Manipal Hospital, Bangalore, India

    Somashekar S. P. & Archa Prasad

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  1. Ashok B. C.
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  2. Harish Kumar Kabilan
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  3. Anantheswar Y. N.
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Correspondence to Harish Kumar Kabilan.

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C., A.B., Kabilan, H.K., N., A.Y. et al. Role of Indocyanine Green in Breast Surgery. Indian J Surg 84 (Suppl 3), 592–601 (2022). https://doi.org/10.1007/s12262-021-03128-y

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