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Laser speckle contrast imaging and quantitative fluorescence angiography for perfusion assessment

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Abstract

Purpose

Indocyanine green fluorescence angiography (ICG-FA) is an established technique for assessment of intestinal perfusion during gastrointestinal surgery, whereas quantitative ICG-FA (q-ICG) and laser speckle contrast imaging (LSCI) are relatively unproven. The study aimed to investigate whether the techniques could be applied interchangeably for perfusion assessment.

Methods

Nineteen pigs underwent laparotomy, two minor resections of the small bowel, and anastomoses. Additionally, seven pigs had parts of their stomach and small intestine de-vascularized. Data was also collected from an in vivo model (inferior caval vein measurements in two additional pigs) and an ex vivo flow model, allowing for standardization of experimental flow, distance, and angulation. Q-ICG and LSCI were performed, so that regions of interest were matched between the two modalities in the analyses, ensuring coverage of the same tissue.

Results

The overall correlation of q-ICG and LSCI evaluated in the porcine model was modest (rho = 0.45, p < 0.001), but high in tissue with low perfusion (rho = 0.74, p < 0.001).

Flux values obtained by LSCI from the ex vivo flow model revealed a decreasing flux with linearly increasing distance as well as angulation to the model. The Q-ICG perfusion values obtained varied slightly with increasing distance as well as angulation to the model.

Conclusions

Q-ICG and LSCI cannot be used interchangeably but may supplement each other. LSCI is profoundly affected by angulation and distance. In comparison, q-ICG is minimally affected by changing experimental conditions and is more readily applicable in minimally invasive surgery.

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Abbreviations

ICG:

Indocyanine green

ICG-FA:

Indocyanine green–fluorescence angiography

LSCI:

Laser speckle contrast imaging

LSPU:

Laser speckle perfusion units

q-ICG:

Quantitative indocyanine green fluorescence angiography

ROI:

Region of interest

RPM:

Revolutions per minute

References

  1. Thompson SK, Chang EY, Jobe BA (2006) Clinical review: healing in gastrointestinal anastomoses, part I. Microsurgery 26:131–136. https://doi.org/10.1002/micr.20197

    Article  PubMed  Google Scholar 

  2. Chadi SA, Fingerhut A, Berho M, DeMeester SR, Fleshman JW, Hyman NH, Margolin DA, Martz JE, McLemore EC, Molena D, Newman MI, Rafferty JF, Safar B, Senagore AJ, Zmora O, Wexner SD (2016) Emerging trends in the etiology, prevention, and treatment of gastrointestinal anastomotic leakage. J Gastrointest Surg 20:2035–2051. https://doi.org/10.1007/s11605-016-3255-3

    Article  PubMed  Google Scholar 

  3. 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 

  4. Kofoed SC, Calatayud D, Jensen LS, Helgstrand F, Achiam MP, De Heer P, Svendsen LB (2015) Intrathoracic anastomotic leakage after gastroesophageal cancer resection is associated with increased risk of recurrence. J Thorac Cardiovasc Surg 150:42–48. https://doi.org/10.1016/j.jtcvs.2015.04.030

    Article  PubMed  Google Scholar 

  5. Kofoed SC, Calatayud D, Jensen LS, Jensen MV, Svendsen LB (2014) Intrathoracic anastomotic leakage after gastroesophageal cancer resection is associated with reduced long-term survival. World J Surg 38:114–119. https://doi.org/10.1007/s00268-013-2245-9

    Article  PubMed  Google Scholar 

  6. 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 disease : the official journal of the Association of. Coloproctol G B Irel 12:1018–1025. https://doi.org/10.1111/j.1463-1318.2009.01944.x

    Article  CAS  Google Scholar 

  7. 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 Color Dis 24:569–576. https://doi.org/10.1007/s00384-009-0658-6

    Article  CAS  Google Scholar 

  8. 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. https://doi.org/10.1097/SLA.0b013e3182128929

    Article  PubMed  Google Scholar 

  9. Jessen M, Nerstrom M, Wilbek TE, Roepstorff S, Rasmussen MS, Krarup PM (2016) Risk factors for clinical anastomotic leakage after right hemicolectomy. Int J Color Dis 31:1619–1624. https://doi.org/10.1007/s00384-016-2623-5

    Article  Google Scholar 

  10. Briers JD, Fercher AF (1982) Retinal blood-flow visualization by means of laser speckle photography. Invest Ophthalmol Vis Sci 22:255–259

    CAS  PubMed  Google Scholar 

  11. Owens SL (1996) Indocyanine green angiography. Br J Ophthalmol 80:263–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Yannuzzi LA, Slakter JS, Sorenson JA, Guyer DR, Orlock DA (2012) Digital indocyanine green videoangiography and choroidal neovascularization. 1992. Retina 32(Suppl 1):191

    Article  PubMed  Google Scholar 

  13. Valdes PA, Roberts DW, Lu FK, Golby A (2016) Optical technologies for intraoperative neurosurgical guidance. Neurosurg Focus 40:E8. https://doi.org/10.3171/2015.12.focus15550

    Article  PubMed  PubMed Central  Google Scholar 

  14. Fredrickson VL, Russin JJ, Strickland BA, Bakhsheshian J, Amar AP (2017) Intraoperative imaging for vascular lesions. Neurosurg Clin N Am 28:603–613. https://doi.org/10.1016/j.nec.2017.05.011

    Article  PubMed  Google Scholar 

  15. Kaiser M, Yafi A, Cinat M, Choi B, Durkin AJ (2011) Noninvasive assessment of burn wound severity using optical technology: a review of current and future modalities. Burns 37:377–386. https://doi.org/10.1016/j.burns.2010.11.012

    Article  PubMed  Google Scholar 

  16. Alander JT, Kaartinen I, Laakso A, Patila T, Spillmann T, Tuchin VV, Venermo M, Valisuo P (2012) A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012:940585. https://doi.org/10.1155/2012/940585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Marano A, Priora F, Lenti LM, Ravazzoni F, Quarati R, Spinoglio G (2013) Application of fluorescence in robotic general surgery: review of the literature and state of the art. World J Surg 37:2800–2811. https://doi.org/10.1007/s00268-013-2066-x

    Article  PubMed  Google Scholar 

  18. Degett TH, Andersen HS, Gogenur I (2016) Indocyanine green fluorescence angiography for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbeck's Arch Surg 401:767–775. https://doi.org/10.1007/s00423-016-1400-9

    Article  Google Scholar 

  19. Nerup N, Andersen HS, Ambrus R, Strandby RB, Svendsen MBS, Madsen MH, Svendsen LB, Achiam MP (2017) Quantification of fluorescence angiography in a porcine model. Langenbeck's Arch Surg 402:655–662. https://doi.org/10.1007/s00423-016-1531-z

    Article  Google Scholar 

  20. Diana M, Agnus V, Halvax P, Liu YY, Dallemagne B, Schlagowski AI, Geny B, Diemunsch P, Lindner V, Marescaux J (2015) Intraoperative fluorescence-based enhanced reality laparoscopic real-time imaging to assess bowel perfusion at the anastomotic site in an experimental model. Br J Surg 102:e169–e176. https://doi.org/10.1002/bjs.9725

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  22. Toens C, Krones CJ, Blum U, Fernandez V, Grommes J, Hoelzl F, Stumpf M, Klinge U, Schumpelick V (2006) Validation of IC-VIEW fluorescence videography in a rabbit model of mesenteric ischaemia and reperfusion. Int J Color Dis 21:332–338. https://doi.org/10.1007/s00384-005-0017-1

    Article  CAS  Google Scholar 

  23. Nadort A, Kalkman K, van Leeuwen TG, Faber DJ (2016) Quantitative blood flow velocity imaging using laser speckle flowmetry. Sci Rep 6:25258. https://doi.org/10.1038/srep25258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Forrester KR, Tulip J, Leonard C, Stewart C, Bray RC (2004) A laser speckle imaging technique for measuring tissue perfusion. IEEE Trans Biomed Eng 51:2074–2084. https://doi.org/10.1109/TBME.2004.834259

    Article  PubMed  Google Scholar 

  25. Senarathna J, Rege A, Li N, Thakor NV (2013) Laser speckle contrast imaging: theory, instrumentation and applications. IEEE Rev Biomed Eng 6:99–110. https://doi.org/10.1109/RBME.2013.2243140

    Article  PubMed  Google Scholar 

  26. Ambrus R, Strandby RB, Svendsen LB, Achiam MP, Steffensen JF, Sondergaard Svendsen MB (2016) Laser speckle contrast imaging for monitoring changes in microvascular blood flow. Eur Surg Res 56:87–96. https://doi.org/10.1159/000442790

    Article  PubMed  Google Scholar 

  27. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412. https://doi.org/10.1371/journal.pbio.1000412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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. https://doi.org/10.1097/SLA.0b013e31828d4ab3

    Article  PubMed  Google Scholar 

  29. Mukaka MM (2012) Statistics corner: a guide to appropriate use of correlation coefficient in medical research. Malawi Med J 24:69–71

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Lee IA, Preacher KJ (2013) Calculation for the test of the difference between two dependent correlations with one variable in common [Computer software]. Available from http://quantpsy.org. Accessed 11 Jan 2018

  31. Steiger JH (1980) Tests for comparing elements of a correlation matrix. Psychol Bull 87:245–251. https://doi.org/10.1037/0033-2909.87.2.245

    Article  Google Scholar 

  32. Davis MA, Kazmi SM, Dunn AK (2014) Imaging depth and multiple scattering in laser speckle contrast imaging. J Biomed Opt 19:086001. https://doi.org/10.1117/1.jbo.19.8.086001

    Article  PubMed  PubMed Central  Google Scholar 

  33. Frangioni JV (2008) New technologies for human cancer imaging. J Clin Oncol 26:4012–4021. https://doi.org/10.1200/jco.2007.14.3065

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ambrus R, Strandby RB, Secher NH, Runitz K, Svendsen MB, Petersen LG, Achiam MP, Svendsen LB (2016) Thoracic epidural analgesia reduces gastric microcirculation in the pig. BMC Anesthesiol 16:86. https://doi.org/10.1186/s12871-016-0256-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Heymann MA, Payne BD, Hoffman JI, Rudolph AM (1977) Blood flow measurements with radionuclide-labeled particles. Prog Cardiovasc Dis 20:55–79

    Article  CAS  PubMed  Google Scholar 

  36. Lange M, Hamahata A, Traber DL, Nakano Y, Traber LD, Enkhbaatar P (2013) Multiple versus single injections of fluorescent microspheres for the determination of regional organ blood flow in septic sheep. Lab Anim 47:203–209. https://doi.org/10.1177/0023677213487718

    Article  CAS  PubMed  Google Scholar 

  37. Reinhardt CP, Dalhberg S, Tries MA, Marcel R, Leppo JA (2001) Stable labeled microspheres to measure perfusion: validation of a neutron activation assay technique. Am J Physiol Heart Circ Physiol 280:H108–H116

    Article  CAS  PubMed  Google Scholar 

  38. Alemanno G, Somigli R, Prosperi P, Bergamini C, Maltinti G, Giordano A, Valeri A (2016) Combination of diagnostic laparoscopy and intraoperative indocyanine green fluorescence angiography for the early detection of intestinal ischemia not detectable at CT scan. Int J Surg Case Rep 26:77–80. https://doi.org/10.1016/j.ijscr.2016.07.016

    Article  PubMed  PubMed Central  Google Scholar 

  39. Shimizu S, Kamiike W, Hatanaka N, Yoshida Y, Tagawa K, Miyata M, Matsuda H (1995) New method for measuring ICG Rmax with a clearance meter. World J Surg 19:113–118 discussion 118

    Article  CAS  PubMed  Google Scholar 

  40. Nerup N, Knudsen KBK, Ambrus R, Svendsen MBS, Thymann T, Ifaoui IBR, Svendsen LB, Achiam MP (2017) Reproducibility and reliability of repeated quantitative fluorescence angiography. Surg Technol Int 31:35–39

    PubMed  Google Scholar 

  41. Quero G, Lapergola A, Barberio M, Seeliger B, Saccomandi P, Guerriero L, Mutter D, Saadi A, Worreth M, Marescaux J, Agnus V, Diana M (2018) Discrimination between arterial and venous bowel ischemia by computer-assisted analysis of the fluorescent signal. Surg Endosc. https://doi.org/10.1007/s00464-018-6512-6

  42. Baiocchi GL, Diana M, Boni L (2018) Indocyanine green-based fluorescence imaging in visceral and hepatobiliary and pancreatic surgery: state of the art and future directions. World J Gastroenterol 24:2921–2930. https://doi.org/10.3748/wjg.v24.i27.2921

    Article  PubMed  PubMed Central  Google Scholar 

  43. Ortega AE, Richman MF, Hernandez M, Peters JH, Anthone GJ, Azen S, Beart RW Jr (1996) Inferior vena caval blood flow and cardiac hemodynamics during carbon dioxide pneumoperitoneum. Surg Endosc 10:920–924

    Article  CAS  PubMed  Google Scholar 

  44. Lindberg F, Bergqvist D, Rasmussen I, Haglund U (1997) Hemodynamic changes in the inferior caval vein during pneumoperitoneum. An experimental study in pigs. Surg Endosc 11:431–437

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The study was sponsored by donations from private foundations, to whom the authors owe gratitude: Mogens Andresen fonden, Civilingeniør Johannes Elmqvist Ormstrup og Hustru Grete Omstrups Fond, and Fabrikant Frands Køhler Nielsens og Hustrus Mindelegat. Sponsors had no role in study design, interpretation of results, or any other part of the study. Also, a sincere thanks to Jens Osterkamp, MD, for the help with illustrations.

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Author notes

  1. Jonas Hedelund Rønn and Nikolaj Nerup have contributed equally to the work, and share first author ship

Authors and Affiliations

  1. Department of Surgical Gastroenterology, Copenhagen University Hospital Rigshospitalet, Blegdamsvej 9, 2100, Copenhagen, Denmark

    Jonas Hedelund Rønn, Nikolaj Nerup, Rune Broni Strandby, Rikard Ambrus, Lars Bo Svendsen & Michael Patrick Achiam

  2. Copenhagen Academy for Medical Education and Simulation, Center for Human Resources, Capital Region of Denmark, Rigshospitalet, Copenhagen, Denmark

    Morten Bo Søndergaard Svendsen

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  1. Jonas Hedelund Rønn
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Contributions

Study conception and design: JHR, NN, LBS, MPA. Acquisition of data: JHR, RA, NN, RBS. Analysis and interpretation of data: JHR, NN, RBS, MBS, RA, LBS, MPA. Drafting of the manuscript: JHR, NN. Critical revision and final approval of the manuscript: JHR, NN, RBS, MBS, RA, LBS, MPA.

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Correspondence to Nikolaj Nerup.

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The authors declare that they have no conflict of interest.

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All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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Rønn, J.H., Nerup, N., Strandby, R.B. et al. Laser speckle contrast imaging and quantitative fluorescence angiography for perfusion assessment. Langenbecks Arch Surg 404, 505–515 (2019). https://doi.org/10.1007/s00423-019-01789-8

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