Pre- and intra-operative imaging techniques for sentinel node localization in breast cancer

Despite the fact that sentinel lymph node biopsy has been accepted worldwide as a highly accurate staging method for solid cancers, some potential intraoperative drawbacks and controversial issues still remain. This article provides an update on innovations for sentinel lymph node mapping and biopsy. Advances in computer technology and data processing make it possible to integrate anatomic and functional images together with 3D rendering systems. This facilitates the lymph node peri-intraoperative localization, especially of the deep-seated ones. Furthermore, it provides an update on advances in the integration of hybrid imaging technologies for the surgical management of patients. Moreover, this review includes the experience on the use of small-field scintigraphic imaging devices to be employed in the surgical room. Evidence is emerging that these devices may improve intraoperative identification of sentinel nodes. Other potential tools, such as radioguided occult lesion localization and radioactive see...

[1]  Thomas Wendler,et al.  Image navigation as a means to expand the boundaries of fluorescence-guided surgery , 2012, Physics in medicine and biology.

[2]  E. Even-Sapir,et al.  Clinical applications of gamma-detection probes – radioguided surgery , 1999, European Journal of Nuclear Medicine.

[3]  S. Toyoshima,et al.  Double mapping with subareolar blue dye and peritumoral green dye injections decreases the false-negative rate of dye-only sentinel node biopsy for early breast cancer: 2-site injection is more accurate than 1-site injection. , 2006, Surgery.

[4]  Tessa Buckle,et al.  Tumor bracketing and safety margin estimation using multimodal marker seeds: a proof of concept. , 2010, Journal of biomedical optics.

[5]  R. V. Valdés Olmos,et al.  Sentinel Node Mapping for Breast Cancer: Current Situation , 2012, Journal of oncology.

[6]  D. Brasse,et al.  A new intraoperative gamma camera for the sentinel lymph node procedure in breast cancer. , 2008, Anticancer research.

[7]  U. Metser,et al.  Lymphoscintigraphic sentinel node identification in patients with breast cancer: the role of SPECT-CT , 2006, European Journal of Nuclear Medicine and Molecular Imaging.

[8]  U. Chetty,et al.  Role of routine preoperative lymphoscintigraphy in sentinel node biopsy for breast cancer. , 2005, European journal of cancer.

[9]  S. Alvarez,et al.  Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. , 2006, AJR. American journal of roentgenology.

[10]  J. Klode,et al.  Radio‐guided surgery: advantages of a new portable γ‐camera (Sentinella®) for intraoperative real time imaging and detection of sentinel lymph nodes in cutaneous malignancies , 2012, Journal of the European Academy of Dermatology and Venereology : JEADV.

[11]  Adverse reaction; patent blue turning patient blue , 2012, BMJ Case Reports.

[12]  E. Rutgers,et al.  Lymphatic mapping and sentinel node biopsy , 1997 .

[13]  V Ntziachristos,et al.  Intraoperative near-infrared fluorescence imaging for sentinel lymph node detection in vulvar cancer: first clinical results. , 2011, Gynecologic oncology.

[14]  M. Kawashima,et al.  Transcutaneous detection and direct approach to the sentinel node using axillary compression technique in ICG fluorescence-navigated sentinel node biopsy for breast cancer , 2012, Breast Cancer.

[15]  A. Balm,et al.  Concomitant radio- and fluorescence-guided sentinel lymph node biopsy in squamous cell carcinoma of the oral cavity using ICG-99mTc-nanocolloid , 2012, European Journal of Nuclear Medicine and Molecular Imaging.

[16]  N. S. van den Berg,et al.  Fluorescence guidance in urologic surgery , 2012, Current Opinion in Urology.

[17]  Nassir Navab,et al.  Towards Intra-operative 3D Nuclear Imaging: Reconstruction of 3D Radioactive Distributions Using Tracked Gamma Probes , 2007, MICCAI.

[18]  S. Heller,et al.  Nuclear probes and intraoperative gamma cameras. , 2011, Seminars in nuclear medicine.

[19]  W. Vogel,et al.  The yield of SPECT/CT for anatomical lymphatic mapping in patients with breast cancer , 2009, European Journal of Nuclear Medicine and Molecular Imaging.

[20]  I. V. D. van der Ploeg,et al.  The efficacy of 'Radio guided Occult Lesion Localization' (ROLL) versus 'Wire-guided Localization' (WGL) in breast conserving surgery for non-palpable breast cancer: A randomized clinical trial – ROLL study , 2008, BMC surgery.

[21]  Renato A. Valdés Olmos,et al.  SPECT/CT and a Portable γ-Camera for Image-Guided Laparoscopic Sentinel Node Biopsy in Testicular Cancer , 2011, The Journal of Nuclear Medicine.

[22]  R. A. Valdés-Olmos,et al.  [Evaluation of the sentinel lymph node combining SPECT/CT with the planar image and its importance for the surgical act]. , 2011, Revista espanola de medicina nuclear.

[23]  D. Huss,et al.  Optimization of sentinel lymph node biopsy in breast cancer using an operative gamma camera , 2007, World journal of surgical oncology.

[24]  G. Wishart,et al.  A feasibility study (ICG-10) of indocyanine green (ICG) fluorescence mapping for sentinel lymph node detection in early breast cancer. , 2012, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[25]  Jos Jonkers,et al.  A self-assembled multimodal complex for combined pre- and intraoperative imaging of the sentinel lymph node , 2010, Nanotechnology.

[26]  Seiya Inoue,et al.  Sentinel Lymph Node Biopsy Using Intraoperative Indocyanine Green Fluorescence Imaging Navigated with Preoperative CT Lymphography for Superficial Esophageal Cancer , 2012, Annals of Surgical Oncology.

[27]  M. Wallis,et al.  Ultrasound guided percutaneous axillary lymph node core biopsy: how often is the sentinel lymph node being biopsied? , 2009, Breast.

[28]  C. Cox,et al.  Localization of non-palpable breast cancer using a radiolabelled titanium seed: van Riet YEA, Jansen FH, van Beek M, et al (Catharina Hosp, Eindhoven, The Netherlands; Univ Hosp, Leiden, The Netherlands) Br J Surg 97:1240-1245, 2010§ , 2011 .

[29]  P. Tanis,et al.  History of sentinel node and validation of the technique , 2001, Breast Cancer Research.

[30]  Sergi Vidal-Sicart,et al.  Added Value of Intraoperative Real-Time Imaging in Searches for Difficult-to-Locate Sentinel Nodes , 2010, The Journal of Nuclear Medicine.

[31]  Milton V. Marshall,et al.  Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study. , 2008, Radiology.

[32]  Michael Hünerbein,et al.  ICG fluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer , 2010, Breast Cancer Research and Treatment.

[33]  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.

[34]  Z. Hall.  Cancer , 1906, The Hospital.

[35]  I. V. D. van der Ploeg,et al.  SPECT/CT for preoperative sentinel node localization , 2010, Journal of surgical oncology.

[36]  J. Ayuso,et al.  [PET/CT-guided salvage surgery protocol. Results with ROLL Technique and PET probe]. , 2011, Revista espanola de medicina nuclear.

[37]  M. Mascalchi,et al.  Predicting the status of axillary lymph nodes in breast cancer: a multiparameter approach including axillary ultrasound scanning. , 2009, Breast.

[38]  S. Muller,et al.  Evaluation of surgical gamma probes for radioguided sentinel node localisation , 1998, European Journal of Nuclear Medicine.

[39]  D L Morton,et al.  Technical details of intraoperative lymphatic mapping for early stage melanoma. , 1992, Archives of surgery.

[40]  D. Murawa,et al.  Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence , 2009, The British journal of surgery.

[41]  J. L. Carreras-Delgado,et al.  Contribution of the portable gamma camera to detect the sentinel node in breast cancer during surgery. , 2012, Revista espanola de medicina nuclear e imagen molecular.

[42]  S. Singletary,et al.  Incidence of anaphylactoid reactions to isosulfan blue dye during breast carcinoma lymphatic mapping in patients treated with preoperative prophylaxis , 2005, Cancer.

[43]  W. Mali,et al.  Preoperative needle biopsy of sentinel lymph nodes using intradermal microbubbles and contrast-enhanced ultrasound in patients with breast cancer. , 2012, AJR. American journal of roentgenology.

[44]  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.

[45]  A. Vahrmeijer,et al.  Dose optimization for near‐infrared fluorescence sentinel lymph node mapping in patients with melanoma , 2013, The British journal of dermatology.

[46]  S. Vidal-Sicart,et al.  [Evaluation of the sentinel lymph node combining SPECT/CT with the planar image and its importance for the surgical act]. , 2011, Revista espanola de medicina nuclear.

[47]  T. Zhao,et al.  Preoperative Lymphoscintigraphy Predicts the Successful Identification but Is Not Necessary in Sentinel Lymph Nodes Biopsy in Breast Cancer , 2007, Annals of Surgical Oncology.

[48]  Jennifer Weeks,et al.  Preoperative sentinel node identification with ultrasound using microbubbles in patients with breast cancer. , 2011, AJR. American journal of roentgenology.

[49]  J. Pavía,et al.  Radioguided occult lesion localisation in breast cancer using an intraoperative portable gamma camera: first results , 2008, European Journal of Nuclear Medicine and Molecular Imaging.

[50]  I. Komenaka,et al.  Occurrence of prolonged injection site mass with methylene blue but not isosulfan blue after the sentinel node procedure. , 2011, Archives of surgery.

[51]  S. Mclaughlin,et al.  A Multi‐site Validation Trial of Radioactive Seed Localization as an Alternative to Wire Localization , 2008, The breast journal.

[52]  Sergi Vidal-Sicart,et al.  The use of a portable gamma camera for preoperative lymphatic mapping: a comparison with a conventional gamma camera , 2011, European Journal of Nuclear Medicine and Molecular Imaging.

[53]  D. Rubello,et al.  Is the "ideal" gamma-probe for intraoperative radioguided surgery conceivable? , 2005, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

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

[55]  Takayuki Kinoshita,et al.  Evaluation of sentinel node biopsy by combined fluorescent and dye method and lymph flow for breast cancer. , 2010, Breast.

[56]  P. Chin,et al.  (Non-targeted) radioactive/fluorescent nanoparticles and their potential in combined pre- and intraoperative imaging during sentinel lymph node resection , 2010, Nanotechnology.

[57]  P. V. van Diest,et al.  Impact of lymphoscintigraphy on sentinel node identification with technetium-99m-colloidal albumin in breast cancer. , 1997, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[58]  E. Rutgers,et al.  Radioguided occult lesion localisation (ROLL) in breast-conserving surgery after neoadjuvant chemotherapy. , 2012, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[59]  Y. Iwasaki,et al.  A Novel Approach for Sentinel Lymph Node Identification Using Fluorescence Imaging and Image Overlay Navigation Surgery in Patients with Breast Cancer , 2016, World Journal of Surgery.

[60]  A. Elola-Olaso,et al.  Contribution of the portable gamma camera to detect the sentinel node in breast cancer during surgery. , 2012 .

[61]  Ur Metser,et al.  Improved sentinel node identification by SPECT/CT in overweight patients with breast cancer. , 2007, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[62]  R. Newcombe,et al.  Adverse reactions to patent blue V dye - The NEW START and ALMANAC experience. , 2010, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[63]  Michael Hünerbein,et al.  Current trends and emerging future of indocyanine green usage in surgery and oncology , 2011, Cancer.

[64]  C. V. D. van de Velde,et al.  Randomized Comparison of Near-infrared Fluorescence Imaging Using Indocyanine Green and 99m Technetium With or Without Patent Blue for the Sentinel Lymph Node Procedure in Breast Cancer Patients , 2012, Annals of Surgical Oncology.

[65]  C. T. de Lara,et al.  Prospective multicentric randomized study comparing periareolar and peritumoral injection of radiotracer and blue dye for the detection of sentinel lymph node in breast sparing procedures: FRANSENODE trial. , 2007, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[66]  H. G. van der Poel,et al.  Comparing the Hybrid Fluorescent–Radioactive Tracer Indocyanine Green–99mTc-Nanocolloid with 99mTc-Nanocolloid for Sentinel Node Identification: A Validation Study Using Lymphoscintigraphy and SPECT/CT , 2012, The Journal of Nuclear Medicine.

[67]  G. Nieuwenhuijzen,et al.  Localization of non‐palpable breast cancer using a radiolabelled titanium seed , 2010, The British journal of surgery.

[68]  D. Murawa,et al.  Breast cancer sentinel lymph node mapping using near infrared guided indocyanine green and indocyanine green--human serum albumin in comparison with gamma emitting radioactive colloid tracer. , 2012, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[69]  Kei Aoyama,et al.  Sentinel lymph node biopsy for breast cancer patients using fluorescence navigation with indocyanine green , 2011, World journal of surgical oncology.

[70]  B. Hesse,et al.  Factors of importance for scintigraphic non-visualisation of sentinel nodes in breast cancer , 2005, European Journal of Nuclear Medicine and Molecular Imaging.

[71]  Sergi Vidal-Sicart,et al.  Technological innovation in the sentinel node procedure: towards 3-D intraoperative imaging , 2010, European Journal of Nuclear Medicine and Molecular Imaging.

[72]  John V Frangioni,et al.  New technologies for human cancer imaging. , 2008, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[73]  A. Alavi,et al.  Current status of sentinel lymph-node biopsy in patients with breast cancer , 2011, European Journal of Nuclear Medicine and Molecular Imaging.

[74]  Hein Putter,et al.  Randomized, double-blind comparison of indocyanine green with or without albumin premixing for near-infrared fluorescence imaging of sentinel lymph nodes in breast cancer patients , 2011, Breast Cancer Research and Treatment.

[75]  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.

[76]  K. McMasters,et al.  Preoperative lymphoscintigraphy for breast cancer does not improve the ability to identify axillary sentinel lymph nodes. , 2000, Annals of surgery.

[77]  Sarfraz Ahmad,et al.  Detection of sentinel lymph nodes in patients with endometrial cancer undergoing robotic-assisted staging: a comparison of colorimetric and fluorescence imaging. , 2012, Gynecologic oncology.

[78]  David Cosgrove,et al.  Ultrasound contrast agents: an overview. , 2006, European journal of radiology.

[79]  Anastasia Ivanova,et al.  Robotically assisted fluorescence-guided lymph node mapping with ICG for gynecologic malignancies: a feasibility study. , 2012, Gynecologic oncology.

[80]  J. Klode,et al.  Indocyanine green fluorescence‐guided sentinel lymph node biopsy in dermato‐oncology , 2012, Journal der Deutschen Dermatologischen Gesellschaft = Journal of the German Society of Dermatology : JDDG.

[81]  Chintamani,et al.  Sentinel lymph node biopsy using dye alone method is reliable and accurate even after neo-adjuvant chemotherapy in locally advanced breast cancer - a prospective study , 2011, World journal of surgical oncology.

[82]  M. Noguchi,et al.  Complement of peritumoral and subareolar injection in breast cancer sentinel lymph node biopsy , 2009, Journal of surgical oncology.

[83]  Tadao Shimizu,et al.  A Comparison of Indocyanine Green Fluorescence Imaging Plus Blue Dye and Blue Dye Alone for Sentinel Node Navigation Surgery in Breast Cancer Patients , 2012, Annals of Surgical Oncology.

[84]  J. Vicente,et al.  Optimización de la biopsia selectiva de ganglio centinela en el cáncer de mama mediante palpación axilar intraoperatoria , 2010 .

[85]  P. Ell,et al.  Sentinel lymph node detection and imaging , 1999, European Journal of Nuclear Medicine.

[86]  M. Soler,et al.  Protocolo de cirugía de rescate guiada por PET/TAC. Resultados con técnica ROLL y sonda PET , 2011 .

[87]  S. Horenblas,et al.  Intraoperative radioguidance with a portable gamma camera: a novel technique for laparoscopic sentinel node localisation in urological malignancies , 2009, European Journal of Nuclear Medicine and Molecular Imaging.

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

[89]  Tomoharu Shimizu,et al.  Indocyanine green fluorescence imaging system for sentinel lymph node biopsies in early breast cancer patients , 2011, Surgery Today.

[90]  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.

[91]  L. Newman,et al.  Lymphatic mapping techniques and sentinel lymph node biopsy in breast cancer. , 2007, The Surgical clinics of North America.

[92]  G. Bisi,et al.  Sentinel lymph node detection in patients with early-stage breast cancer: comparison of periareolar and subdermal/peritumoral injection techniques. , 2004, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[93]  Tessa Buckle,et al.  Dual-emissive quantum dots for multispectral intraoperative fluorescence imaging. , 2010, Biomaterials.

[94]  V. Kanakala,et al.  Clinical and histopathological factors affecting failed sentinel node localization in axillary staging for breast cancer. , 2013, The surgeon : journal of the Royal Colleges of Surgeons of Edinburgh and Ireland.

[95]  J. Duch,et al.  Portable gamma cameras: the real value of an additional view in the operating theatre , 2011, European Journal of Nuclear Medicine and Molecular Imaging.

[96]  Kensuke Kawasaki,et al.  Evaluation of Breast Lymphatic Pathways with Indocyanine Green Fluorescence Imaging in Patients with Breast Cancer , 2008, World Journal of Surgery.

[97]  A. Balm,et al.  Feasibility of Sentinel Node Biopsy in Head and Neck Melanoma Using a Hybrid Radioactive and Fluorescent Tracer , 2011, Annals of Surgical Oncology.

[98]  Michael Hünerbein,et al.  Ultrastaging of colon cancer by sentinel node biopsy using fluorescence navigation with indocyanine green , 2012, International Journal of Colorectal Disease.

[99]  Ricardo Bonomi,et al.  Comparison of radioguided occult lesion localization (ROLL) and wire localization for non‐palpable breast cancers: A meta‐analysis , 2012, Journal of surgical oncology.

[100]  J. Thompson,et al.  Mammary lymphoscintigraphy in breast cancer. , 1995, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[101]  Michael V Knopp,et al.  A comprehensive overview of radioguided surgery using gamma detection probe technology , 2009, World journal of surgical oncology.

[102]  A. Spillane,et al.  Patent Blue V dye anaphylaxis: experience of Australian and New Zealand surgeons , 2014, ANZ journal of surgery.

[103]  D. Krag,et al.  The False-Negative Rate of Sentinel Node Biopsy in Patients with Breast Cancer: A Meta-Analysis , 2012, World Journal of Surgery.

[104]  R. A. Valdés Olmos,et al.  Sentinel Node Detection in Head and Neck Malignancies: Innovations in Radioguided Surgery , 2009, Journal of oncology.

[105]  Nassir Navab,et al.  First demonstration of 3-D lymphatic mapping in breast cancer using freehand SPECT , 2010, European Journal of Nuclear Medicine and Molecular Imaging.

[106]  David W Townsend,et al.  Procedure Guideline for SPECT/CT Imaging 1.0. , 2006, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[107]  T. Yeatman,et al.  Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. , 1996, JAMA.

[108]  I. B. Borel Rinkes,et al.  Efficacy of ‘radioguided occult lesion localisation’ (ROLL) versus ‘wire-guided localisation’ (WGL) in breast conserving surgery for non-palpable breast cancer: a randomised controlled multicentre trial , 2012, Breast Cancer Research and Treatment.

[109]  M. Knopp,et al.  Combined approach of perioperative 18F-FDG PET/CT imaging and intraoperative 18F-FDG handheld gamma probe detection for tumor localization and verification of complete tumor resection in breast cancer , 2007, World journal of surgical oncology.

[110]  Philip Varghese,et al.  Methylene Blue Dye—A Safe and Effective Alternative for Sentinel Lymph Node Localization , 2008, The breast journal.

[111]  D. Rubello,et al.  Is the “Ideal” γ-Probe for Intraoperative Radioguided Surgery Conceivable? , 2005 .

[112]  R. Mansel,et al.  Does imaging in sentinel node scintigraphic localization add value to the procedure in patients with breast cancer? , 2005, Nuclear medicine communications.

[113]  D. Eshima,et al.  Lymphoscintigraphy, the sentinel node concept, and the intraoperative gamma probe in melanoma, breast cancer, and other potential cancers. , 1997, Seminars in nuclear medicine.

[114]  Lenka Vermeeren,et al.  Intraoperative Imaging for Sentinel Node Identification in Prostate Carcinoma: Its Use in Combination with Other Techniques , 2011, The Journal of Nuclear Medicine.

[115]  T. Kinoshita,et al.  Sentinel lymph node biopsy in breast cancer patients with previous breast augmentation surgery , 2014, Breast Cancer.

[116]  M. Keshtgar,et al.  Establishing axillary Sentinel Lymph Node Biopsy (SLNB) for early breast cancer in the United Kingdom: a survey of the national training program. , 2009, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[117]  W. Studer,et al.  Anaphylaxis to isosulfan blue and cross-reactivity to patent blue V: case report and review of the nomenclature of vital blue dyes. , 2006, Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology.

[118]  G. Mariani,et al.  General Concepts on Radioguided Sentinel Lymph Node Biopsy: Preoperative Imaging, Intraoperative Gamma-Probe Guidance, Intraoperative Imaging, and Multimodality Imaging , 2013 .

[119]  J. Maublant,et al.  Sentinel node in breast cancer procedural guidelines , 2007 .

[120]  F. Moffat.  Targeting gold at the end of the rainbow: Surgical gamma probes in the 21st century , 2007, Journal of surgical oncology.