Image-guided hepatopancreatobiliary surgery using near-infrared fluorescent light

BackgroundImproved imaging methods and surgical techniques have created a new era in hepatopancreatobiliary (HPB) surgery. Despite these developments, visual inspection, palpation, and intraoperative ultrasound remain the most utilized tools during surgery today. This is problematic, though, especially in laparoscopic HPB surgery, where palpation is not possible. Optical imaging using near-infrared (NIR) fluorescence can be used for the real-time assessment of both anatomy (e.g., sensitive detection and demarcation of tumours and vital structures) and function (e.g., assessment of luminal flow and tissue perfusion) during both open and minimally invasive surgeries.MethodsThis article reviews the published literature related to preclinical development and clinical applications of NIR fluorescence imaging during HPB surgery.ResultsNIR fluorescence imaging combines the use of otherwise invisible NIR fluorescent contrast agents and specially designed camera systems, which are capable of detecting these contrast agents during surgery. Unlike visible light, NIR fluorescent light can penetrate several millimetres through blood and living tissue, thus providing improved detectability. Applications of this technique during HPB surgery include tumour imaging in liver and pancreas, and real-time imaging of the biliary tree.ConclusionsNIR fluorescence imaging is a promising new technique that may someday improve surgical accuracy and lower complications.

[1]  Sylvain Gioux,et al.  Real-time, near-infrared, fluorescence-guided identification of the ureters using methylene blue. , 2010, Surgery.

[2]  Giuseppe Garcea,et al.  Survival following curative resection for pancreatic ductal adenocarcinoma. A systematic review of the literature. , 2008, JOP : Journal of the pancreas.

[3]  Osamu Ishikawa,et al.  A novel image‐guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation , 2009, Journal of surgical oncology.

[4]  J. Ferlay,et al.  Global Cancer Statistics, 2002 , 2005, CA: a cancer journal for clinicians.

[5]  H. Maeda,et al.  Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. , 2000, Journal of controlled release : official journal of the Controlled Release Society.

[6]  H. Yamaue,et al.  Combined intraoperative use of contrast-enhanced ultrasonography imaging using a sonazoid and fluorescence navigation system with indocyanine green during anatomical hepatectomy , 2011, Langenbeck's Archives of Surgery.

[7]  A. Jemal,et al.  Cancer Statistics, 2010 , 2010, CA: a cancer journal for clinicians.

[8]  K. Sugimachi,et al.  Bile Leakage After Hepatic Resection , 2001, Annals of surgery.

[9]  Frcsc Paul D. Greig MD,et al.  Survival After Hepatic Resection for Colorectal Metastases: A 10-Year Experience , 2006, Annals of Surgical Oncology.

[10]  A. Jemal,et al.  Global Cancer Statistics , 2011 .

[11]  S. Yamada,et al.  Prognostic Factors for Survival After Extended Pancreatectomy for Pancreatic Head Cancer: Influence of Resection Margin Status on Survival , 2009, Pancreas.

[12]  T. T. White,et al.  Cholangiography and small duct injury. , 1985, American journal of surgery.

[13]  A. Kwon,et al.  Intraoperative indocyanine green fluorescent imaging for prevention of bile leakage after hepatic resection. , 2011, Surgery.

[14]  J. Bookstein,et al.  Differential Problems in the Angiographie of Carcinoma the Pancreas1 , 1970 .

[15]  W. Mali,et al.  Rapid Visualization of Human Tumor Xenografts through Optical Imaging with a Near-Infrared Fluorescent Anti–Epidermal Growth Factor Receptor Nanobody , 2012, Molecular imaging.

[16]  E. Kwok,et al.  Use of Methylene Blue in Sepsis: A Systematic Review , 2006, Journal of intensive care medicine.

[17]  J. Stedeford,et al.  Neurological sequelae following methylene blue injection for parathyroidectomy , 2003, Anaesthesia.

[18]  David A Boas,et al.  Comparison of frequency-domain and time-domain fluorescence lifetime tomography. , 2008, Optics letters.

[19]  S. Gabriel,et al.  Systematic Review of the Literature , 2021, Adherence to Antiretroviral Therapy among Perinatal Women in Guyana.

[20]  Takeaki Ishizawa,et al.  Real‐time identification of liver cancers by using indocyanine green fluorescent imaging , 2009, Cancer.

[21]  Akira Makino,et al.  Near-infrared fluorescence tumor imaging using nanocarrier composed of poly(L-lactic acid)-block-poly(sarcosine) amphiphilic polydepsipeptide. , 2009, Biomaterials.

[22]  V. Dest,et al.  When the diagnosis is pancreatic cancer. , 1991, RN.

[23]  Tessa Buckle,et al.  Intraoperative laparoscopic fluorescence guidance to the sentinel lymph node in prostate cancer patients: clinical proof of concept of an integrated functional imaging approach using a multimodal tracer. , 2011, European urology.

[24]  Hiroshi Imamura,et al.  Intraoperative fluorescent cholangiography using indocyanine green: a biliary road map for safe surgery. , 2009, Journal of the American College of Surgeons.

[25]  R. Schaffer,et al.  The White test: a new dye test for intraoperative detection of bile leakage during major liver resection. , 2008, Archives of surgery.

[26]  Hisataka Kobayashi,et al.  Toxicity of Organic Fluorophores Used in Molecular Imaging: Literature Review , 2009, Molecular imaging.

[27]  Y Bandai,et al.  Indocyanine green‐fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience , 2010 .

[28]  Alexander L. Vahrmeijer,et al.  Optical Image-guided Surgery—Where Do We Stand? , 2010, Molecular Imaging and Biology.

[29]  W. Fawcett,et al.  Survival and recurrence after neo-adjuvant chemotherapy and liver resection for colorectal metastases: a ten year study. , 2009, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[30]  Tatsuo Igarashi,et al.  Usefulness of intraoperative fluorescence imaging to evaluate local anatomy in hepatobiliary surgery , 2008, Journal of hepato-biliary-pancreatic surgery.

[31]  Tatsuya Aoki,et al.  Ultrasonography-guided hepatic tumor resection using a real-time virtual sonography with indocyanine green navigation (with videos) , 2011, Journal of hepato-biliary-pancreatic sciences.

[32]  G. Kwant,et al.  Light-absorbing properties, stability, and spectral stabilization of indocyanine green. , 1976, Journal of applied physiology.

[33]  G. Stamp,et al.  Survival analysis after pancreatic resection for ampullary and pancreatic head carcinoma: An analysis of clinicopathological factors , 2009, Journal of surgical oncology.

[34]  Ken Hayashi,et al.  Image-Guided Liver Mapping Using Fluorescence Navigation System with Indocyanine Green for Anatomical Hepatic Resection , 2008, World Journal of Surgery.

[35]  Yasuhiko Sugawara,et al.  Application of fluorescent cholangiography to single-incision laparoscopic cholecystectomy , 2011, Surgical Endoscopy.

[36]  M. Makuuchi,et al.  Randomized trial of the usefulness of a bile leakage test during hepatic resection. , 2000, Archives of surgery.

[37]  H. Maeda,et al.  A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. , 1986, Cancer research.

[38]  J. Fleshman,et al.  Liver resection for colorectal metastases. , 2004, Annals of the Royal College of Surgeons of England.

[39]  Sylvain Gioux,et al.  Wavelength optimization for rapid chromophore mapping using spatial frequency domain imaging. , 2010, Journal of biomedical optics.

[40]  J. M. Anderson,et al.  Selective parathyroid and pancreatic staining , 1969, The British journal of surgery.

[41]  T. Pawlik,et al.  Combined Resection and Radiofrequency Ablation for Advanced Hepatic Malignancies: Results in 172 Patients , 2003, Annals of Surgical Oncology.

[42]  M. Hutteman,et al.  Near-Infrared Fluorescence Imaging in Patients Undergoing Pancreaticoduodenectomy , 2011, European Surgical Research.

[43]  R. Schirmer,et al.  “Lest we forget you — methylene blue …” , 2011, Neurobiology of Aging.

[44]  M. Sinanan,et al.  Common bile duct injury during laparoscopic cholecystectomy and the use of intraoperative cholangiography: adverse outcome or preventable error? , 2001, Archives of surgery.

[45]  Ralph Weissleder,et al.  Intraoperative Near-Infrared Fluorescent Cholangiography (NIRFC) in Mouse Models of Bile Duct Injury , 2010, World Journal of Surgery.

[46]  H. Yamaue,et al.  Combined Use of Contrast-Enhanced Intraoperative Ultrasonography and a Fluorescence Navigation System for Identifying Hepatic Metastases , 2010, World Journal of Surgery.

[47]  H. Putter,et al.  Near-infrared fluorescence imaging of liver metastases in rats using indocyanine green. , 2012, The Journal of surgical research.

[48]  Randomized clinical trial of routine on‐table cholangiography during laparoscopic cholecystectomy , 2011, The British journal of surgery.

[49]  Yasuhiko Sugawara,et al.  Hepatobiliary surgery guided by a novel fluorescent imaging technique for visualizing hepatic arteries, bile ducts, and liver cancers on color images. , 2011, Journal of the American College of Surgeons.

[50]  G. Stansby,et al.  Intraoperative Ultrasonographic Imaging in Liver Surgery: A Review , 1990, HPB surgery : a world journal of hepatic, pancreatic and biliary surgery.

[51]  Sharmeela Kaushal,et al.  Fluorescence laparoscopy imaging of pancreatic tumor progression in an orthotopic mouse model , 2010, Surgical Endoscopy.

[52]  Jouke Dijkstra,et al.  Image-guided tumor resection using real-time near-infrared fluorescence in a syngeneic rat model of primary breast cancer , 2011, Breast Cancer Research and Treatment.

[53]  M. Hutteman,et al.  Intraoperative near-infrared fluorescence imaging of colorectal metastases targeting integrin α(v)β(3) expression in a syngeneic rat model. , 2011, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[54]  Kenneth Hess,et al.  Recurrence and Outcomes Following Hepatic Resection, Radiofrequency Ablation, and Combined Resection/Ablation for Colorectal Liver Metastases , 2004, Annals of surgery.

[55]  T. Ishizawa,et al.  Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: an initial experience. , 2009, Archives of surgery.

[56]  K. Kusaka,et al.  Fluorescence navigation hepatectomy by visualization of localized cholestasis from bile duct tumor infiltration. , 2010, Journal of the American College of Surgeons.

[57]  Erlong Zhang,et al.  A review of NIR dyes in cancer targeting and imaging. , 2011, Biomaterials.

[58]  R. Baldessarini,et al.  Neurosyphilis, Malaria, and the Discovery of Antipsychotic Agents , 2008, Harvard review of psychiatry.

[59]  J. Bookstein,et al.  Differential problems in the angiographic diagnosis of carcinoma of the pancreas. , 1970, Radiology.

[60]  M. Kusano,et al.  Intraoperative fluorescent imaging using indocyanine green for liver mapping and cholangiography , 2010, Journal of hepato-biliary-pancreatic sciences.

[61]  John V Frangioni,et al.  Real-time assessment of cardiac perfusion, coronary angiography, and acute intravascular thrombi using dual-channel near-infrared fluorescence imaging. , 2009, The Journal of thoracic and cardiovascular surgery.

[62]  M. Osman,et al.  Decreased Blood Flow with Increased Metabolic Activity: A Novel Sign of Pancreatic Tumor Aggressiveness , 2009, Clinical Cancer Research.

[63]  David A. Cheresh,et al.  Role of integrins in cell invasion and migration , 2002, Nature Reviews Cancer.

[64]  Merlijn Hutteman,et al.  The clinical use of indocyanine green as a near‐infrared fluorescent contrast agent for image‐guided oncologic surgery , 2011, Journal of surgical oncology.

[65]  Shohachi Suzuki,et al.  Bile leak test by indocyanine green fluorescence images after hepatectomy. , 2010, American journal of surgery.

[66]  N. Dubrawsky Cancer statistics , 1989, CA: a cancer journal for clinicians.

[67]  K. Hasegawa,et al.  Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy , 2010, The British journal of surgery.

[68]  Sylvain Gioux,et al.  Real-time intra-operative near-infrared fluorescence identification of the extrahepatic bile ducts using clinically available contrast agents. , 2010, Surgery.

[69]  Hak Soo Choi,et al.  Real-time intraoperative assessment of the extrahepatic bile ducts in rats and pigs using invisible near-infrared fluorescent light. , 2008, Surgery.

[70]  Michael A. Choti,et al.  1423 pancreaticoduodenectomies for pancreatic cancer: A single-institution experience , 2006, Journal of Gastrointestinal Surgery.

[71]  Hak Soo Choi,et al.  Intraoperative Localization of Insulinoma and Normal Pancreas Using Invisible Near-Infrared Fluorescent Light , 2010, Annals of Surgical Oncology.

[72]  J. Frangioni,et al.  Image-Guided Surgery Using Invisible Near-Infrared Light: Fundamentals of Clinical Translation , 2010, Molecular imaging.

[73]  L. Ngo,et al.  The FLARE™ Intraoperative Near-Infrared Fluorescence Imaging System: A First-in-Human Clinical Trial in Breast Cancer Sentinel Lymph Node Mapping , 2009, Annals of Surgical Oncology.

[74]  A. Meining,et al.  Highly sensitive detection of early‐stage pancreatic cancer by multimodal near‐infrared molecular imaging in living mice , 2008, International journal of cancer.

[75]  S Mizuno,et al.  Indocyanine Green (ICG) Fluorescence Imaging‐Guided Cholangiography for Donor Hepatectomy in Living Donor Liver Transplantation , 2010, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[76]  A. Jemal,et al.  Global cancer statistics , 2011, CA: a cancer journal for clinicians.

[77]  Sylvain Gioux,et al.  Toward Optimization of Imaging System and Lymphatic Tracer for Near-Infrared Fluorescent Sentinel Lymph Node Mapping in Breast Cancer , 2011, Annals of Surgical Oncology.

[78]  Mitsugi Shimoda,et al.  Intraoperative exploration of biliary anatomy using fluorescence imaging of indocyanine green in experimental and clinical cholecystectomies , 2010, Journal of hepato-biliary-pancreatic sciences.