Skip to main content
SpringerLink
Log in

ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Fluorescence technology with indocyanine green (ICG) provides a real-time assessment of intestinal perfusion. However, a subjective evaluation of fluorescence intensity based on the surgeon’s visual judgement is a major limitation. This study evaluated the quantitative assessment of ICG fluorescence imaging in determining the transection line of the proximal colon during laparoscopic colorectal surgery.

Methods

This is a retrospective analysis of a prospectively maintained database of 112 patients who underwent laparoscopic surgery for left-sided colorectal cancers. After distal transection of the bowel, the specimen was extracted extracorporeally and then the proximal colon was divided within the well-perfused area based on the ICG fluorescence imaging. We evaluated whether quantitative assessment of intestinal perfusion by measuring ICG intensity could predict postoperative outcomes: F max, T max, T 1/2, and Slope were calculated.

Results

Anastomotic leakage (AL) occurred in 5 cases (4.5%). Based on the fluorescence imaging, the surgical team opted for further proximal change of the transection line up to an “adequate” fluorescent portion in 18 cases (16.1%). Among the 18 patients, AL occurred in 4 patients (4/18: 22.2%), whereas it occurred in only 1 case (1/94: 1.0%) in the good perfusion patients who did not need proximal change of the transection line. The F max of the AL group was less than 52.0 in all 5 cases (5/5), whereas that of the non-AL group was in only 8 cases (8/107): with an F max cutoff value of 52.0, the sensitivity and specificity for the prediction of AL were 100 and 92.5%, respectively. Regarding postoperative bowel movement recovery, the T max of the early flatus group or early defecation group was significantly lower than that of the late flatus group or late defecation group, respectively.

Conclusions

ICG fluorescence imaging is useful for assessing anastomotic perfusion in colorectal surgery, which can result in more precise operative decisions tailored for an individual patient.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Kingham TP, Pachter HL (2009) Colonic anastomotic leak: risk factors, diagnosis, and treatment. J Am Coll Surg 208:269–278

    Article  PubMed  Google Scholar 

  2. Branagan G, Finnis D; Wessex Colorectal Cancer Audit Working Group (2005) Prognosis after anastomotic leakage in colorectal surgery. Dis Colon Rectum 48:1021–1026

    Article  PubMed  Google Scholar 

  3. Mirnezami A, Mirnezami R, Chandrakumaran K, Sasapu K, Sagar P, Finan P (2011) Increased local recurrence and reduced survival from colorectal cancer following anastomotic leak: systematic review and meta-analysis. Ann Surg 253:890–899

    Article  PubMed  Google Scholar 

  4. Kang CY, Halabi WJ, Chaudhry OO, Nguyen V, Pigazzi A, Carmichael JC, Mills S, Stamos MJ (2013) Risk factors for anastomotic leakage after anterior resection for rectal cancer. JAMA Surg 148:65–71

    Article  PubMed  Google Scholar 

  5. Qu H, Liu Y, Bi DS (2015) Clinical risk factors for anastomotic leakage after laparoscopic anterior resection for rectal cancer: a systematic review and meta-analysis. Surg Endosc 29:3608–3617

    Article  PubMed  Google Scholar 

  6. Shiomi A, Ito M, Maeda K, Kinugasa Y, Ota M, Yamaue H, Shiozawa M, Horie H, Kuriu Y, Saito N (2015) Effects of a diverting stoma on symptomatic anastomotic leakage after low anterior resection for rectal cancer: a propensity score matching analysis of 1,014 consecutive patients. J Am Coll Surg 220:186–194

    Article  PubMed  Google Scholar 

  7. Matsubara N, Miyata H, Gotoh M, Tomita N, Baba H, Kimura W, Nakagoe T, Simada M, Kitagawa Y, Sugihara K, Mori M (2014) Mortality after common rectal surgery in Japan: a study on low anterior resection from a newly established nationwide large-scale clinical database. Dis Colon Rectum 57:1075–1081

    Article  PubMed  Google Scholar 

  8. Vignali A, Gianotti L, Braga M, Radaelli G, Malvezzi L, Di Carlo V (2000) Altered microperfusion at the rectal stump is predictive for rectal anastomotic leak. Dis Colon Rectum 43:76–82

    Article  CAS  PubMed  Google Scholar 

  9. Sheridan WG, Lowndes RH, Young HL (1987) Tissue oxygen tension as a predictor of colonic anastomotic healing. Dis Colon Rectum 30:867–871

    Article  CAS  PubMed  Google Scholar 

  10. Kologlu M, Yorganci K, Renda N, Sayek I (2000) Effect of local and remote ischemia-reperfusion injury on healing of colonic anastomoses. Surgery 128:99–104

    Article  CAS  PubMed  Google Scholar 

  11. Kawada K, Sakai Y (2016) Preoperative, intraoperative and postoperative risk factors for anastomotic leakage after laparoscopic low anterior resection with double stapling technique anastomosis. World J Gastroenterol 22:5718–5727

    Article  PubMed  PubMed Central  Google Scholar 

  12. Nakayama S, Hasegawa S, Nagayama S, Kato S, Hida K, Tanaka E, Itami A, Kubo H, Sakai Y (2011) The importance of precompression time for secure stapling with a linear stapler. Surg Endosc 25:2382–2386

    Article  PubMed  Google Scholar 

  13. Nakayama S, Hasegawa S, Hida K, Kawada K, Sakai Y (2015) Obtaining secure stapling of a double stapling anastomosis. J Surg Res 193:652–657

    Article  PubMed  Google Scholar 

  14. Hasegawa S, Nakayama S, Hida K, Kawada K, Sakai Y (2015) Effect of tri-staple™ technology and slow firing on secure stapling using an endoscopic linear stapler. Dig Surg 32:353–360

    Article  PubMed  Google Scholar 

  15. Kawada K, Hasegawa S, Hida K, Hirai K, Okoshi K, Nomura A, Kawamura J, Nagayama S, Sakai Y (2014) Risk factors for anastomotic leakage after laparoscopic low anterior resection with DST anastomosis. Surg Endosc 28:2988–2995

    Article  PubMed  PubMed Central  Google Scholar 

  16. Karliczek A, Harlaar NJ, Zeebregts CJ, Wiggers T, Baas PC, van Dam GM (2009) Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis 24:569–576

    Article  CAS  PubMed  Google Scholar 

  17. Kudszus S, Roesel C, Schachtrupp A, Hoer JJ (2010) Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbecks Arch Surg 395:1025–1030

    Article  PubMed  Google Scholar 

  18. Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, Stamos MJ, Pigazzi A (2013) The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 27:3003–3008

    Article  PubMed  Google Scholar 

  19. Hellan M, Spinoglio G, Pigazzi A, Lagares-Garcia JA (2014) The influence of fluorescence imaging on the location of bowel transection during robotic left-sided colorectal surgery. Surg Endosc 28:1695–1702

    Article  PubMed  Google Scholar 

  20. Jafari MD, Wexner SD, Martz JE, McLemore EC, Margolin DA, Sherwinter DA, Lee SW, Senagore AJ, Phelan MJ, Stamos MJ (2015) Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg 220:82–92

    Article  PubMed  Google Scholar 

  21. Degett TH, Andersen HS, Gögenur I (2016) Indocyanine green fluorescence angiography for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbecks Arch Surg 401:767–775

    Article  PubMed  Google Scholar 

  22. Kawada K, Hasegawa S, Wada T, Takahashi R, Hisamori S, Hida K, Sakai Y (2016) Evaluation of intestinal perfusion by ICG fluorescence imaging in laparoscopic colorectal surgery with DST anastomosis. Surg Endosc :1–9

  23. Sakai Y, Kitano S (2015) Practice guidelines on endoscopic surgery for qualified surgeons by the endoscopic surgical skill qualification system. Asian J Endosc Surg 8:103–113

    Article  PubMed  Google Scholar 

  24. Hasegawa S, Nagayama S, Nomura A, Kawamura J, Sakai Y (2008) Multimedia article. Autonomic nerve-preserving total mesorectal excision in the laparoscopic era. Dis Colon Rectum 51:1279–1282

    Article  PubMed  Google Scholar 

  25. Kuroyanagi H, Oya M, Ueno M, Fujimoto Y, Yamaguchi T, Muto T (2008) Standardized technique of laparoscopic intracorporeal rectal transection and anastomosis for low anterior resection. Surg Endosc 22:557–561

    Article  PubMed  Google Scholar 

  26. Araki J, Nishizawa Y, Nakamura T, Sato T, Naito M, Fujii S, Mihara M, Koshima I (2012) The development of a canine anorectal autotransplantation model based on blood supply: a preliminary case report. PLoS ONE 7:e44310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kawaguchi Y, Ishizawa T, Miyata Y, Yamashita S, Masuda K, Satou S, Tamura S, Kaneko J, Sakamoto Y, Aoki T, Hasegawa K, Sugawara Y, Kokudo N (2013) Portal uptake function in veno-occlusive regions evaluated by real-time fluorescent imaging using indocyanine green. J Hepatol 58:247–253

    Article  PubMed  Google Scholar 

  28. Terasaki H, Inoue Y, Sugano N, Jibiki M, Kudo T, Lepäntalo M, Venermo M (2013) A quantitative method for evaluating local perfusion using indocyanine green fluorescence imaging. Ann Vasc Surg 27:1154–1161

    Article  PubMed  Google Scholar 

  29. Igari K, Kudo T, Uchiyama H, Toyofuku T, Inoue Y (2014) Intraarterial injection of indocyanine green for evaluation of peripheral blood circulation in patients with peripheral arterial disease. Ann Vasc Surg 28:1280–1285

    Article  PubMed  Google Scholar 

  30. Kawaguchi Y, Tanaka N, Nagai M, Nomura Y, Fuks D, Gayet B, Kokudo N (2015) Usefulness of intraoperative real-time tissue elastography during laparoscopic hepatectomy. J Am Coll Surg 221:e103-e111

    Google Scholar 

  31. Kamiya K, Unno N, Miyazaki S, Sano M, Kikuchi H, Hiramatsu Y, Ohta M, Yamatodani T, Mineta H, Konno H (2015) Quantitative assessment of the free jejunal graft perfusion. J Surg Res 194:394–399

    Article  PubMed  Google Scholar 

  32. Venermo M, Settembre N, Albäck A, Vikatmaa P, Aho PS, Lepäntalo M, Inoue Y, Terasaki H (2016) Pilot assessment of the repeatability of indocyanine green fluorescence imaging and correlation with traditional foot perfusion assessments. Eur J Vasc Endovasc Surg 52:527–533

    Article  CAS  PubMed  Google Scholar 

  33. Ambrosetti P, Robert J, Mathey P, Rohner A (1994) Left-sided colon and colorectal anastomoses: Doppler ultrasound as an aid to assess bowel vascularization. A prospective evaluation of 200 consecutive elective cases. Int J Colorectal Dis 9:211–214

    Article  CAS  PubMed  Google Scholar 

  34. Boyle NH, Manifold D, Jordan MH, Mason RC (2000) Intraoperative assessment of colonic perfusion using scanning laser Doppler flowmetry during colonic resection. J Am Coll Surg 191:504–510

    Article  CAS  PubMed  Google Scholar 

  35. Karliczek A, Benaron DA, Baas PC, Zeebregts CJ, Wiggers T, van Dam GM (2010) Intraoperative assessment of microperfusion with visible light spectroscopy for prediction of anastomotic leakage in colorectal anastomoses. Colorectal Dis 12:1018–1025

    Article  CAS  PubMed  Google Scholar 

  36. Still J, Law E, Dawson J, Bracci S, Island T, Holtz J (1999) Evaluation of the circulation of reconstructive flaps using laser-induced fluorescence of indocyanine green. Ann Plast Surg 42:266–274

    Article  CAS  PubMed  Google Scholar 

  37. Waseda K, Ako J, Hasegawa T, Shimada Y, Ikeno F, Ishikawa T, Demura Y, Hatada K, Yock PG, Honda Y, Fitzgerald PJ, Takahashi M (2009) Intraoperative fluorescence imaging system for on-site assessment of off-pump coronary artery bypass graft. JACC Cardiovasc Imaging 2:604–612

    Article  PubMed  Google Scholar 

  38. Yukaya T, Saeki H, Kasagi Y, Nakashima Y, Ando K, Imamura Y, Ohgaki K, Oki E, Morita M, Maehara Y (2015) Indocyanine green fluorescence angiography for quantitative evaluation of gastric tube perfusion in patients undergoing esophagectomy. J Am Coll Surg 221:e37–e42

    Article  PubMed  Google Scholar 

  39. Kin C, Vo H, Welton L, Welton M (2015) Equivocal effect of intraoperative fluorescence angiography on colorectal anastomotic leaks. Dis Colon Rectum 58:582–587

    Article  PubMed  Google Scholar 

  40. Boni L, Fingerhut A, Marzorati A, Rausei S, Dionigi G, Cassinotti E (2016) Indocyanine green fluorescence angiography during laparoscopic low anterior resection: results of a case-matched study. Surg Endosc:1–5

  41. Matsui A, Winer JH, Laurence RG, Frangioni JV (2011) Predicting the survival of experimental ischaemic small bowel using intraoperative near-infrared fluorescence angiography. Br J Surg 98:1725–1734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V, Soler L, Barry B, Namer IJ, Demartines N, Charles AL, Geny B, Marescaux J (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank medical staffs and residents of Kyoto University Hospital gastrointestinal surgery for their participation in this study. We could not have completed the study without their diligence and support. We also thank Mr. Takahiro Shikayama (Hamamatsu Photonics K.K.) for technical assistance for the analysis using ROIs. We would like to thank Editage (http://www.editage.jp) for English language editing.

Author information

Authors and Affiliations

  1. Department of Surgery, Graduate School of Medicine, Kyoto University, 54 Shogoin- Kawara-cho, Sakyo-ku, Kyoto, 606-8507, Japan

    Toshiaki Wada, Kenji Kawada, Ryo Takahashi, Mami Yoshitomi, Koya Hida & Yoshiharu Sakai

  2. Department of Gastroenterological Surgery, Fukuoka University Faculty of Medicine, Fukuoka, Japan

    Suguru Hasegawa

Authors
  1. Toshiaki Wada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kenji Kawada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ryo Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mami Yoshitomi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Koya Hida
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Suguru Hasegawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yoshiharu Sakai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenji Kawada.

Ethics declarations

Disclosure

Drs. Toshiaki Wada, Kenji Kawada, Ryo Takahashi, Mami Yoshitomi, Koya Hida, Suguru Hasegawa, and Yoshiharu Sakai have no conflicts of interest or financial ties to disclose.

Additional information

T. Wada and K. Kawada contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

464_2017_5475_MOESM1_ESM.jpg

Supplementary Figure 1. A) Bowel perfusion under white/visible light. Forceps was placed at the transection line. B) Bowel perfusion under ICG fluorescence imaging. Three regions of interest (ROIs) were labeled as followed: Point 1 (mesenteric side of the transection line), Point 2 (midpoint of the transection line) and Point 3 (antimesenteric side of the transection line). C) Time curve of ICG fluorescence intensity. Point 1 is a red curve, Point 2 is a blue curve, and Point 3 is a green curve. (JPG 480 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wada, T., Kawada, K., Takahashi, R. et al. ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surg Endosc 31, 4184–4193 (2017). https://doi.org/10.1007/s00464-017-5475-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-017-5475-3

Keywords

Search

Navigation