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Qiu W, Zhou C, Zhao W, Mei S, Liu Q. ICG fluorescence-guided sentinel lymph node biopsy for decision-making in lateral lymph node dissection in local advanced rectal cancer: a retrospective study. Updates Surg 2025:10.1007/s13304-025-02169-2. [PMID: 40205080 DOI: 10.1007/s13304-025-02169-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/13/2025] [Accepted: 03/05/2025] [Indexed: 04/11/2025]
Abstract
Local advanced rectal cancer (LARC) carries high recurrence risks, especially with lateral lymph node (LLN) involvement. This study aims to evaluate the role of ICG-guided sentinel lymph node biopsy (SLNB) in patients with clinical negative LLNs (maximum diameter < 7 mm), potentially reducing unnecessary surgeries and associated complications in patients with LARC. A retrospective analysis of 301 consecutive patients with lower LARC who underwent fluorescent lateral pelvic sentinel lymph node biopsy (FL-SLNB) or conventional LLND at the Cancer Hospital, Chinese Academy of Medical Sciences between 2018 and 2022 was conducted. Clinical and pathological data were collected, and the patients were grouped into FL-SLNB and non-SLNB groups. Postoperative complications, recurrence rates, and survival outcomes were assessed. Statistical analysis was performed using χ2 tests, Mann-Whitney U tests, Kaplan-Meier survival curves, and Cox proportional hazards models. FL-SLNB (173 patients) showed better perioperative outcomes than non-SLNB (128 patients), with shorter hospital stays (7 vs. 10 days, P = 0.027), less blood loss (150 vs. 180 mL, P = 0.032), and fewer complications: intraoperative bleeding (2.9% vs. 6.3%, P = 0.041), anastomotic leakage (1.7% vs. 3.9%, P = 0.045), and urinary dysfunction (3.5% vs. 7.0%, P = 0.039). No significant differences were observed in survival or recurrence rates (P > 0.05). pN stage was a significant predictor of distant metastasis (HR 1.953, P = 0.037). ICG-guided SLNB enhanced surgical precision and reduced unnecessary LLND in lower LARC with clinically negative LLNs, and improved surgical decision-making and minimizes postoperative complications.
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Affiliation(s)
- Wenlong Qiu
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, People's Republic of China
| | - Cheng Zhou
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, People's Republic of China
| | - Wei Zhao
- Department of Colorectal Surgery, Tianjin Union Medical Center, Tianjin, People's Republic of China
- The Institute of Translational Medicine, Tianjin Union Medical Center of Nankai University, Tianjin, People's Republic of China
- Tianjin Institute of Coloproctology, Tianjin, People's Republic of China
| | - Shiwen Mei
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, People's Republic of China
| | - Qian Liu
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, People's Republic of China.
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Ochiai K, Ishihara S. Surgical navigation for lateral pelvic lymph node dissection in rectal cancer. Tech Coloproctol 2025; 29:63. [PMID: 39937208 DOI: 10.1007/s10151-024-03084-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/14/2024] [Accepted: 11/25/2024] [Indexed: 02/13/2025]
Abstract
Lateral pelvic lymph node dissection (LPLND) provides oncologic benefits in patients with rectal cancer who have enlarged lateral nodes. However, anatomical complexity in the lateral pelvis makes the procedure technically challenging, which may lead to increased intraoperative blood loss, prolonged operative time, postoperative complications and incomplete lymph node dissection. To address such technical challenges, various surgical navigation tools have been developed. In this up-to-date narrative review, we summarize the current evidence on surgical navigation for LPLND and discuss their advantages, limitations and future perspectives.
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Affiliation(s)
- K Ochiai
- Department of Surgical Oncology, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan
- Department of Colon and Rectal Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
| | - S Ishihara
- Department of Surgical Oncology, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan.
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Brollo PP, Stecca T, DI Giacomo A, Massani M, Bresadola V. Near-infrared imaging with indocyanine green fluorescence for intraoperative lymphatic assessment in rectal cancer surgery: a systematic review. Minerva Surg 2025; 80:86-94. [PMID: 40059606 DOI: 10.23736/s2724-5691.25.10731-4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 05/13/2025]
Abstract
INTRODUCTION At present, harvesting more lymph nodes is considered more conducive to the prognosis of colorectal cancer surgery. The recent development of enhanced surgical visualization has led to the wide employment of indocyanine green (ICG) to assist minimally invasive surgery. This systematic review aims to provide a wide and critical overview of the current state of the art of ICG lymphography during rectal surgery, by focusing on the most relevant literature on this topic. EVIDENCE ACQUISITION After validation and registration in the PROSPERO international prospective register of systematic reviews on the 5th May 2024 (ID: CRD42024539426), 8 publications have been considered relevant for the research query and have been divided into two groups: lateral pelvic lymph node dissection (LPLND) and lateral pelvic sentinel lymph node biopsy (LPSLNB). A meta-analysis has not been performed due to the low statistical significance. EVIDENCE SYNTHESIS ICG lymphography seems to improve the number of harvested lateral pelvic lymph nodes, to reduce intraoperative blood loss and hospital length of stay during LPLND. In LPSLNB the detection rate of lateral pelvic sentinel lymph nodes ranged from 91.3% to 92%. CONCLUSIONS ICG lymphography for fluorescence guidance for LLND is a feasible and safe technique, with promising application in terms of the number of harvested lymph nodes and post-operative outcomes improvement during rectal oncological surgery. As some of these benefits have been already suggested by the current literature, they need to be confirmed in larger and randomized clinical.
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Affiliation(s)
- Pier Paolo Brollo
- First General Surgery Unit, Surgery Department, HPB Regional Referral Center, Azienda ULSS2 Marca Trevigiana, Treviso, Italy -
| | - Tommaso Stecca
- First General Surgery Unit, Surgery Department, HPB Regional Referral Center, Azienda ULSS2 Marca Trevigiana, Treviso, Italy
| | - Adriana DI Giacomo
- First General Surgery Unit, Surgery Department, HPB Regional Referral Center, Azienda ULSS2 Marca Trevigiana, Treviso, Italy
| | - Marco Massani
- First General Surgery Unit, Surgery Department, HPB Regional Referral Center, Azienda ULSS2 Marca Trevigiana, Treviso, Italy
| | - Vittorio Bresadola
- General Surgery Department and Simulation Center, Department of Medicine, Academic Hospital of Udine, University of Udine, Udine, Italy
- General Surgery Department, Hospital of San Daniele del Friuli, Udine, Italy
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Negrut RL, Cote A, Feder B, Bodog FD, Maghiar AM. Enhanced Lymph Node Detection in Colon Cancer Using Indocyanine Green Fluorescence: A Systematic Review of Studies from 2020 Onwards. J Pers Med 2025; 15:54. [PMID: 39997331 PMCID: PMC11855940 DOI: 10.3390/jpm15020054] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/06/2024] [Revised: 01/13/2025] [Accepted: 01/27/2025] [Indexed: 02/26/2025] Open
Abstract
Background: Colon cancer is known as one of the most prevalent malignancies in the world. This well-known pathology requires accurate lymph node dissection to achieve effective staging and improved treatment outcomes. Indocyanine green fluorescence imaging has been used as a new technique for enhancing lymph node visualization during surgical intervention. The high rates of local recurrence in colon cancer patients require innovative methods to improve lymphatic mapping and lymph node dissection. This review evaluates the clinical utility and efficacy of ICG imaging in enhancing lymph node accuracy in colon cancer surgery. Materials and methods: A systematic search was conducted in October 2024 (last day of consulting the database was 16 November) across Web of Science, Scopus, and PubMed to identify studies published from 2020 onwards focusing on the use of indocyanine green in colon cancer surgeries. The search terms used were "indocyanine green", "ICG", "fluorescent imaging", "near-infrared imaging", "colon cancer", "colorectal cancer", "colon carcinoma"," colon neoplasms", "surgery", "surgical procedure", "surgical resection", surgical precision". The search followed PRISMA guidelines. The records underwent a two-phase independent screening process conducted by the authors, first based on the title and abstract, followed by full record evaluation. Articles were excluded following certain exclusion criteria: non-human studies; restricted access publications; other publication type than article (review, meta-analysis, questionnaire-based study, case report, etc.), studies focusing on other diseases or studies that focused on the surgical treatment of metastasis from colon cancer; foreign language (non-English); no data of interest for the current review; studies that focused on rectal cancer and that grouped rectal and colon cancer. Data extraction involved both quantitative and qualitative data, such as detection rates, sensitivity, specificity, and other surgical outcomes. Risk of bias was assessed using ROBINS-I, J Joanna Briggs Institute (JBI) Critical Appraisal Checklist, and the Newcastle-Ottawa Scale, depending on study type. The study was not preregistered in PROSPERO. However, to ensure methodological rigor and transparency, it was retrospectively registered in Open Science Framework (OSF). Results: From the 3300 records initially identified, 9 studies were included in this review. Detection rates varied from 55% to 100%, with the highest rate reported in robot-assisted surgeries. The studies showed an improved lymph node detection and lymphatic flow accuracy using ICG fluorescence. Discussion: ICG fluorescence demonstrated substantial benefits, improving staging accuracy and potentially reducing recurrence rates by guiding the lymphadenectomy. The variability observed in detection rates is largely attributed to differences in ICG administration, cancer stage, and surgical approaches. Conclusions: ICG-guided surgery for colon cancer represents a promising advancement, enhancing lymph node detection and staging accuracy. Large-scale randomized trials are essential to establish standardized protocols and validate the efficacy in improving surgical outcomes.
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Affiliation(s)
- Roxana Loriana Negrut
- Department of Medicine, Doctoral School of Biomedical Sciences, Faculty of Medicine and Pharmacy, University of Oradea, 410087 Oradea, Romania; (R.L.N.)
- County Clinical Emergency Hospital Bihor, 410087 Oradea, Romania;
- Department of Surgical Disciplines, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania
| | - Adrian Cote
- County Clinical Emergency Hospital Bihor, 410087 Oradea, Romania;
- Department of Surgical Disciplines, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania
| | - Bogdan Feder
- County Clinical Emergency Hospital Bihor, 410087 Oradea, Romania;
- Department of Surgical Disciplines, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania
| | - Florian Dorel Bodog
- Department of Medicine, Doctoral School of Biomedical Sciences, Faculty of Medicine and Pharmacy, University of Oradea, 410087 Oradea, Romania; (R.L.N.)
- County Clinical Emergency Hospital Bihor, 410087 Oradea, Romania;
- Department of Surgical Disciplines, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania
| | - Adrian Marius Maghiar
- Department of Medicine, Doctoral School of Biomedical Sciences, Faculty of Medicine and Pharmacy, University of Oradea, 410087 Oradea, Romania; (R.L.N.)
- Department of Surgical Disciplines, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania
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Sun L, Meng C, Zhang Z, Luo Y, Yang Z, Yao H. Opportunities and challenges of indocyanine green in gastrointestinal cancers for intraoperative and nano-medicine application. Cancer Nanotechnol 2024; 15:12. [DOI: 10.1186/s12645-024-00251-9] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/08/2023] [Accepted: 01/24/2024] [Indexed: 01/12/2025] Open
Abstract
AbstractThe morbidity and mortality of gastrointestinal tumours remain high worldwide. Surgical resection is currently the most critical radical therapeutic schedule, while postoperative complications and sentinel lymph node (SLN) identification are closely related to the outcome. Indocyanine green (ICG)-mediated fluorescence imaging is increasingly being used in gastrointestinal surgery. It has been embraced by various surgical disciplines as a potential method to improve lymph node detection and enhance surgical field visualization. ICG can passively concentrate in SLN because of enhanced permeation and retention effects. After excitation by near-infrared light devices, SLN can display higher intensity fluorescence, helping visualization for better lymph node dissection. In addition, visual assessment of intestinal blood flow through ICG may reduce the incidence of anastomotic leakage. Although it has good clinical application, ICG-imaging still faces some problems, such as a higher false-negative rate, poorly targeted biodistribution, and lower fluorescence contrast, due to the lack of active tumour targeting. Thus, different ICG-coupled nanoparticles with inherent characteristics or functional modification-enhanced SLN identification features for gastrointestinal cancers bring benefit through active tumour targeting, superior tumour-background ratio, and high resolution. Nano-ICG combined with potential substances, including enhanced imaging contrast and/or combination therapy (chemotherapy, targeted therapy, immunotherapy, etc.), have been packaged and accumulated in the tumour area through active targeting for multimodal imaging and treatment. In this review, we outline the intraoperative application and possible future nanodirections of ICG in gastrointestinal cancer. The prospects and challenges of nano-ICG diagnostic and therapeutic methods in clinical applications are also discussed.
Graphical Abstract
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Sueda T, Yasui M, Nishimura J, Kagawa Y, Kitakaze M, Mori R, Noura S, Omori T, Miyata H, Ohue M. Prognostic impact of lateral sentinel lymph node biopsy using indocyanine green on oncological outcomes for clinical stage II/III lower rectal cancer without suspected lateral lymph node metastasis. Langenbecks Arch Surg 2024; 409:311. [PMID: 39422803 DOI: 10.1007/s00423-024-03501-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/01/2024] [Accepted: 10/09/2024] [Indexed: 10/19/2024]
Abstract
PURPOSE Sentinel lymph node biopsy (SLNB) can detect occult nodal metastasis. We have previously reported the safety and feasibility of indocyanine green (ICG)-guided SLNB for clinical stage II/III lower rectal cancer (RC). However, little is known about the influence of lateral pelvic SLNB using ICG on oncological outcomes. The present study aimed to evaluate the prognostic impact of lateral pelvic SLNB on oncological outcomes compared with prophylactic lateral lymph node dissection (LLND). METHODS Participants comprised consecutive patients with clinical stage II/III lower RC who underwent lateral pelvic SLNB or prophylactic LLND (Non-SLNB) between January 2010 and December 2020. The primary outcome measure was the 5-year cumulative incidence of local recurrence (LR). Secondary endpoints included cancer-specific survival (CSS), overall survival (OS), recurrence-free survival (RFS), local recurrence-free survival (LRFS), and distant recurrence-free survival (DRFS). RESULTS Among the 150 eligible patients included, 79 patients underwent lateral pelvic SLNB. Of those 79 patients, 4 patients who were SLNB-positive underwent LLND. LLND was omitted for the 75 patients who were SLNB-negative. Median follow-up was 61.0 months (range, 1.3-143.2 months). The overall recurrence rate was 30.7% (46 patients), with LR in 12.0% (18 patients). LR comprised lateral lymph node recurrence in 2.6% and central pelvic recurrence in 9.4%. No significant differences were seen between groups in terms of the frequency of LR or in CSS, OS, RFS, LRFS, or DRFS. CONCLUSION Oncological outcomes were not different between the SLNB and Non-SLNB groups. ICG-guided SLNB appears promising as a method for determining indications for LLND.
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Affiliation(s)
- Toshinori Sueda
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan.
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, 3-1-69 Ootemae-Chuoku, Osaka, 540-0008, Japan.
| | - Masayoshi Yasui
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan
| | - Junichi Nishimura
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan
| | - Yoshinori Kagawa
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan
| | - Masatoshi Kitakaze
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan
| | - Ryota Mori
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan
| | - Shingo Noura
- Department of Gastroenterological Surgery, Sakai City Medical Center, Osaka, Japan
| | - Takeshi Omori
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan
| | - Hiroshi Miyata
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan
| | - Masayuki Ohue
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Osaka, Japan
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Brookes MJ, Chan CD, Crowley TP, Ragbir M, Ghosh KM, Beckingsale T, Rankin KS. Intraoperative near-infrared fluorescence guided surgery using indocyanine green (ICG) may aid the surgical removal of benign bone and soft tissue tumours. Surg Oncol 2024; 55:102091. [PMID: 38833894 DOI: 10.1016/j.suronc.2024.102091] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/18/2024] [Revised: 04/08/2024] [Accepted: 05/27/2024] [Indexed: 06/06/2024]
Abstract
BACKGROUND Benign bone and soft tissue tumours encompass a broad, heterogenous range of tumours with varying clinical characteristics. These are often managed surgically with either curettage or marginal excision, but unfortunately have high rates of local recurrence. Indocyanine green (ICG) is a fluorescent dye which can be used to identify solid malignancies intraoperatively but its use is not yet established in benign bone and soft tissue tumours. This study aims to assess whether these tumours fluoresce when administered with ICG pre-operatively and whether this helps surgeons to identify tumour intra-operatively. PATIENTS AND METHODS Patients with locally aggressive benign bone and soft tissue tumours were administered with 25-75 mg of ICG preoperatively at the induction of anaesthesia. Fluorescence was imaged intraoperatively using the Stryker SPY-PHI camera. RESULTS Of the 12 patients included, 11 tumours fluoresced. The surgeons felt the fluorescence guided the procedure in 7 out of the 11 cases which fluoresced. It was felt to be particularly useful in the curettage of bone tumours, in which curettage could be repeated until the absence of fluorescence on imaging. After 12 months, no patients had local recurrence of the tumour. There were no adverse events recorded in this study and surgeons found the technology acceptable. CONCLUSIONS The use of ICG for fluorescence guided surgery is a promising technology to improve outcomes of surgery for benign bone and soft tissue tumours. Further, longer term, study with a control arm is needed to identify whether it results in a reduction in the local recurrence rate.
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Affiliation(s)
- Marcus J Brookes
- North of England Bone and Soft Tissue Tumour Service, Royal Victoria Infirmary, Queen Victoria Road, Newcastle Upon Tyne NE1 4LP, UK; Translational and Clinical Research Institute, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK.
| | - Corey D Chan
- North of England Bone and Soft Tissue Tumour Service, Royal Victoria Infirmary, Queen Victoria Road, Newcastle Upon Tyne NE1 4LP, UK; Translational and Clinical Research Institute, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK
| | - Timothy P Crowley
- North of England Bone and Soft Tissue Tumour Service, Royal Victoria Infirmary, Queen Victoria Road, Newcastle Upon Tyne NE1 4LP, UK
| | - Maniram Ragbir
- North of England Bone and Soft Tissue Tumour Service, Royal Victoria Infirmary, Queen Victoria Road, Newcastle Upon Tyne NE1 4LP, UK
| | - Kanishka M Ghosh
- North of England Bone and Soft Tissue Tumour Service, Royal Victoria Infirmary, Queen Victoria Road, Newcastle Upon Tyne NE1 4LP, UK
| | - Thomas Beckingsale
- North of England Bone and Soft Tissue Tumour Service, Royal Victoria Infirmary, Queen Victoria Road, Newcastle Upon Tyne NE1 4LP, UK
| | - Kenneth S Rankin
- North of England Bone and Soft Tissue Tumour Service, Royal Victoria Infirmary, Queen Victoria Road, Newcastle Upon Tyne NE1 4LP, UK; Translational and Clinical Research Institute, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK
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Morales-Conde S, Navarro-Morales L, Moreno-Suero F, Balla A, Licardie E. Fluorescence and tracers in surgery: the coming future. Cir Esp 2024; 102 Suppl 1:S45-S60. [PMID: 38851317 DOI: 10.1016/j.cireng.2024.05.011] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/07/2024] [Accepted: 05/23/2024] [Indexed: 06/10/2024]
Abstract
The revolution that we are seeing in the world of surgery will determine the way we understand surgical approaches in coming years. Since the implementation of minimally invasive surgery, innovations have constantly been developed to allow the laparoscopic approach to go further and be applied to more and more procedures. In recent years, we have been in the middle of another revolutionary era, with robotic surgery, the application of artificial intelligence and image-guided surgery. The latter includes 3D reconstructions for surgical planning, virtual reality, holograms or tracer-guided surgery, where ICG-guided fluorescence has provided a different perspective on surgery. ICG has been used to identify anatomical structures, assess tissue perfusion, and identify tumors or tumor lymphatic drainage. But the most important thing is that this technology has come hand in hand with the potential to develop other types of tracers that will facilitate the identification of tumor cells and ureters, as well as different light beams to identify anatomical structures. These will lead to other types of systems to assess tissue perfusion without the use of tracers, such as hyperspectral imaging. Combined with the upcoming introduction of ICG quantification, these developments represent a real revolution in the surgical world. With the imminent implementation of these technological advances, a review of their clinical application in general surgery is timely, and this review serves that aim.
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Affiliation(s)
- Salvador Morales-Conde
- Servicio de Cirugía General y Digestiva, Hospital Universitario Virgen Macarena, Facultad de Medicina, Universidad de Sevilla, Sevilla, Spain; Servicio de Cirugía General y Digestiva, Hospital Quironsalud Sagrado Corazón, Sevilla, Spain.
| | - Laura Navarro-Morales
- Servicio de Cirugía General y Digestiva, Hospital Quironsalud Sagrado Corazón, Sevilla, Spain.
| | - Francisco Moreno-Suero
- Servicio de Cirugía General y Digestiva, Hospital Quironsalud Sagrado Corazón, Sevilla, Spain.
| | - Andrea Balla
- Servicio de Cirugía General y Digestiva, Hospital Universitario Virgen Macarena, Facultad de Medicina, Universidad de Sevilla, Sevilla, Spain; Servicio de Cirugía General y Digestiva, Hospital Quironsalud Sagrado Corazón, Sevilla, Spain.
| | - Eugenio Licardie
- Servicio de Cirugía General y Digestiva, Hospital Universitario Virgen Macarena, Facultad de Medicina, Universidad de Sevilla, Sevilla, Spain; Servicio de Cirugía General y Digestiva, Hospital Quironsalud Sagrado Corazón, Sevilla, Spain.
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Kehagias D, Lampropoulos C, Bellou A, Kehagias I. The use of indocyanine green for lateral lymph node dissection in rectal cancer-preliminary data from an emerging procedure: a systematic review of the literature. Tech Coloproctol 2024; 28:53. [PMID: 38761271 PMCID: PMC11102372 DOI: 10.1007/s10151-024-02930-6] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/12/2023] [Accepted: 04/03/2024] [Indexed: 05/20/2024]
Abstract
INTRODUCTION Lateral lymph node dissection (LLND) for rectal cancer is still not a widely established technique owing to the existing controversy between Eastern and Western countries and the lack of well-designed studies. The risk of complications and the paucity of long-term oncological results are significant drawbacks for further applying this technique. The use of indocyanine green (ICG) near-infrared (NIR) fluorescence for LLND appears as a promising technique for enhancing postoperative and oncological outcomes. This review aims to evaluate the emerging role of ICG during LLND and present the benefits of its application. MATERIALS AND METHODS Systematic electronic research was conducted in PubMed and Google Scholar using a combination of medical subject headings (MeSH). Studies presenting the use of ICG during LLND, especially in terms of harvested lymph nodes, were included and reviewed. Studies comparing LLND with ICG (LLND + ICG) or without ICG (LLND-alone) were further analyzed for the number of lymph nodes and postoperative outcomes. RESULTS In total, 13 studies were found eligible and analyzed for different parameters. LLND + ICG is associated with significantly increased number of harvested lateral lymph nodes (p < 0.05), minor blood loss, decreased operative time, and probably decreased urinary retention postoperatively compared with LLND-alone. CONCLUSIONS The use of ICG fluorescence during LLND is a safe and feasible technique for balancing postoperative outcomes and the number of harvested lymph nodes. Well-designed studies with long-term results are required to elucidate the oncological benefits and establish this promising technique.
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Affiliation(s)
- D Kehagias
- Department of General Surgery, General University Hospital of Patras, University of Patras, 26504, Rio, Greece.
| | - C Lampropoulos
- Intensive Care Unit, Saint Andrew's General Hospital, 26335, Patras, Greece
| | - A Bellou
- Intensive Care Unit, Department of Anesthesiology and Intensive Care Medicine, General University Hospital of Patras, 26504, Rio, Greece
| | - I Kehagias
- Department of General Surgery, General University Hospital of Patras, 26504, Rio, Greece
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Varanese M, Arcieri S, Lauro A, Panetta C, Eberspacher C, Palma R, Mascagni D, Pontone S. Indocyanine Green Tattooing During Colonoscopy as a Guide to Laparoscopic Colorectal Cancer Surgery: A Literature Review. Surg Innov 2024; 31:103-110. [PMID: 37923725 DOI: 10.1177/15533506231209127] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/06/2023]
Abstract
BACKGROUND Endoscopic tattooing of colorectal lesions has been performed employing several markers. The indocyanine green (ICG) that uses near infrared fluorescence technology, has been recently adopted in laparoscopic colorectal cancer surgery. This study aims to systematically review the international literature to validate the ICG in laparoscopic colorectal surgery, in order to include the ICG in the therapeutic protocol. METHODS Following AMSTAR 2 criteria, we performed a systematic review to evaluate the use of green indocyanine as a marker for preoperative endoscopic tattooing and for lymph nodes mapping. The study selection was conducted using the PubMed database from January 1989 to July 2022. RESULTS We identified 25 eligible studies. 13 based on fluorescent tumor localization in laparoscopic colorectal surgery using ICG while 12 of them reported the lymphatic road mapping and sentinel node identification by ICG using a near-infrared camera system. One study analyzed both topics. CONCLUSIONS In laparoscopic colorectal cancer surgery indocyanine green can be used to localize fluorescent tumors and mapping fluorescence lymph node. The use of ICG appears to be a valid and safe technique that helps the surgeon to achieve a better oncological radicality. However, the protocols need to be clarified by further studies.
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Affiliation(s)
- Marzia Varanese
- Department of Surgery, Sapienza University of Rome, Rome, Italy
| | - Stefano Arcieri
- Department of Surgery, Sapienza University of Rome, Rome, Italy
| | - Augusto Lauro
- Department of Surgery, Sapienza University of Rome, Rome, Italy
| | | | | | - Rossella Palma
- Department of Surgery, Sapienza University of Rome, Rome, Italy
| | | | - Stefano Pontone
- Department of Surgery, Sapienza University of Rome, Rome, Italy
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Jung JM, Park IJ, Park EJ, Son GM. Fluorescence-guided colorectal surgery: applications, clinical results, and protocols. Ann Surg Treat Res 2023; 105:252-263. [PMID: 38023438 PMCID: PMC10648611 DOI: 10.4174/astr.2023.105.5.252] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/29/2023] [Revised: 10/09/2023] [Accepted: 10/10/2023] [Indexed: 12/01/2023] Open
Abstract
In recent years, the rise of minimally invasive surgery has driven the development of surgical devices. Indocyanine green (ICG) fluorescence imaging is receiving increased attention in colorectal surgery for improved intraoperative visualization and decision-making. ICG, approved by the U.S. Food and Drug Administration in 1959, rapidly binds to plasma proteins and is primarily intravascular. ICG absorption of near-infrared light (750-800 nm) and emission as fluorescence (830 nm) when bound to tissue proteins enhances deep tissue visualization. Applications include assessing anastomotic perfusion, identifying sentinel lymph nodes, and detecting colorectal cancer metastasis. However, standardized protocols and research on clinical outcomes remain limited. This study explores ICG's role, advantages, disadvantages, and potential clinical impact in colorectal surgery.
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Affiliation(s)
- Jin-Min Jung
- Division of Colon and Rectal Surgery, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - In Ja Park
- Division of Colon and Rectal Surgery, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Eun Jung Park
- Division of Colon and Rectal Surgery, Department of Surgery, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
| | - Gyung Mo Son
- Department of Surgery, Pusan National University Yangsan Hospital, Pusan National University School of Medicine, Yangsan, Korea
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Baldari L, Boni L, Cassinotti E. Lymph node mapping with ICG near-infrared fluorescence imaging: technique and results. MINIM INVASIV THER 2023; 32:213-221. [PMID: 37261486 DOI: 10.1080/13645706.2023.2217916] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/16/2023] [Accepted: 05/18/2023] [Indexed: 06/02/2023]
Abstract
PURPOSE Lymphadenectomy represents a fundamental step during gastrointestinal cancer resection, as the removal of an adequate number of lymph nodes is crucial to define the stage of the disease and prognosis. Lymphadenectomy during gastric and colorectal resection and adrenalectomy for cancer are technically demanding and can be associated with risk of bleeding. To date, lymphadenectomy is often performed without any visual aid. Indocyanine green fluorescence for lymph node mapping can provide better intraoperative visualization. The purpose of this review is to report the current evidence on this topic. MATERIALS AND METHODS A systematic research of the electronic databases Medline, Embase and Google Scholar was conducted from the inception to December 2022. RESULTS This review summarizes the current evidence of techniques and results of fluorescence guided lymphatic mapping during gastrointestinal and adrenal surgery. CONCLUSION According to this review, ICG guided lymphadenectomy for gastrointestinal tumours and adrenocortical carcinoma is feasible and safe. In gastrointestinal tumours it allows higher number of harvested lymph nodes.
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Affiliation(s)
- Ludovica Baldari
- Department of General and Minimally Invasive Surgery, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy
| | - Luigi Boni
- Department of General and Minimally Invasive Surgery, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy
| | - Elisa Cassinotti
- Department of General and Minimally Invasive Surgery, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy
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Yao S, Lan H, Han Y, Mao C, Yang M, Zhang X, Jin K. From organ preservation to selective surgery: How immunotherapy changes colorectal surgery? Surg Open Sci 2023; 15:44-53. [PMID: 37637243 PMCID: PMC10450522 DOI: 10.1016/j.sopen.2023.07.024] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2023] [Accepted: 07/29/2023] [Indexed: 08/29/2023] Open
Abstract
The emergence of immunotherapy has revolutionized the traditional treatment paradigm of colorectal cancer (CRC). Among them, immune checkpoint blockade has become the first-line treatment for metastatic colorectal cancer (mCRC) and has made significant progress in the treatment of locally advanced colorectal cancer (LACRC). We reviewed a series of clinical trials that have made breakthrough progress. We will emphasize the breakthrough progress in achieving organ preservation in patients with high microsatellite instability or DNA mismatch repair deficiency (MSI-H/dMMR), and based on this, we propose the concept of selective surgery, which includes selectively removing or preserving lymph nodes, with the aim of proving our idea through more research in the future.
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Affiliation(s)
- Shiya Yao
- Department of Colorectal Surgery, Affiliated Jinhua Hospital, Zhejiang University School of Medicine, Jinhua, Zhejiang 321000, China
| | - Huanrong Lan
- Department of Surgical Oncology, Hangzhou Cancer Hospital, Hangzhou, Zhejiang 310002, China
| | - Yuejun Han
- Department of Colorectal Surgery, Affiliated Jinhua Hospital, Zhejiang University School of Medicine, Jinhua, Zhejiang 321000, China
| | - Chunsen Mao
- Department of Colorectal Surgery, Affiliated Jinhua Hospital, Zhejiang University School of Medicine, Jinhua, Zhejiang 321000, China
| | - Mengxiang Yang
- Department of Colorectal Surgery, Affiliated Jinhua Hospital, Zhejiang University School of Medicine, Jinhua, Zhejiang 321000, China
| | - Xuan Zhang
- Department of Colorectal Surgery, Yunnan Cancer Hospital, The Third Affiliated Hospital of Kunming Medical University, Kunming, Yunnan 650106, China
| | - Ketao Jin
- Department of Colorectal Surgery, Affiliated Jinhua Hospital, Zhejiang University School of Medicine, Jinhua, Zhejiang 321000, China
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Garoufalia Z, Wexner SD. Indocyanine Green Fluorescence Guided Surgery in Colorectal Surgery. J Clin Med 2023; 12:jcm12020494. [PMID: 36675423 PMCID: PMC9865296 DOI: 10.3390/jcm12020494] [Citation(s) in RCA: 24] [Impact Index Per Article: 12.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/21/2022] [Revised: 01/04/2023] [Accepted: 01/04/2023] [Indexed: 01/11/2023] Open
Abstract
BACKGROUND Indocyanine green (ICG) imaging has been increasingly used for intraoperative guidance in colorectal surgery over the past decade. The aim of this study was to review and organize, according to different type of use, all available literature on ICG guided colorectal surgery and highlight areas in need of further research and discuss future perspectives. METHODS PubMed, Scopus, and Google Scholar databases were searched systematically through November 2022 for all available studies on fluorescence-guided surgery in colorectal surgery. RESULTS Available studies described ICG use in colorectal surgery for perfusion assessment, ureteral and urethral assessment, lymphatic mapping, and hepatic and peritoneal metastases assessment. Although the level of evidence is low, results are promising, especially in the role of ICG in reducing anastomotic leaks. CONCLUSIONS ICG imaging is a safe and relatively cheap imaging modality in colorectal surgery, especially for perfusion assessment. Work is underway regarding its use in lymphatic mapping, ureter identification, and the assessment of intraperitoneal metastatic disease.
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Deng J, Hu W, Li Y, Xiong K, Yue T, Lai X, Xiao T. Meta analysis of indocyanine green fluorescence in patients undergoing laparoscopic colorectal cancer surgery. Front Oncol 2022; 12:1010122. [PMID: 36387166 PMCID: PMC9645423 DOI: 10.3389/fonc.2022.1010122] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/08/2022] [Accepted: 10/03/2022] [Indexed: 11/15/2023] Open
Abstract
This meta-analysis intended to systematically evaluate the clinical implications of indocyanine green fluorescence (ICG) in patients undergoing laparoscopic colorectal surgery. PubMed, MEDLINE, Cochrane Library, EMBASE, China National Knowledge Infrastructure (CNKI), Wanfang Database, VIP Medical Information System and China Biomedical Database were synthetically searched for studies published from inception to April 14, 2022. The randomized controlled trials comparing ICG-use with controls were selected. The incidence of anastomotic leakage (AL), lymph node detection, operation duration, intraoperative bleeding, postoperative morbidity, and hospitalization time were evaluated in summary analysis, and calculated the corresponding 95% confidence intervals (CI). Subsequently, in addition to subgroup analyses, studies for heterogeneity, sensitivity, and publication bias were carried out. Consequently, 3453 patients in the enrolled 15 studies were included; 1616 patients were allocated to the experimental group, and 1837 patients were assigned to the control group. The ICG group had a significantly decreased risk of AL (RR: 0.50, 95% CI: 0.37-0.67) and shorter hospitalization time (SMD: -0.31, 95% CI: -0.54-0.08) compared to the control group. Meanwhile, the ICG showed clearly better lymph node detection (SMD: 0.19, 95% CI: 0.02-0.36). However, when the content of operation duration (SMD: -0.07, 95% CI: -0.30-0.15) and intraoperative bleeding (SMD: -0.16, 95% CI: -0.35-0.04) were compared, no statistical significance was found. Furthermore, the pooled analysis of postoperative morbidity was not statistically significant (RR:0.79, 95% CI: 0.58-1.08). The results of the subgroup analysis of AL indicated that there may be regional variations in AL (RR: 0.50, 95% CI: 0.37-0.67) but not in postoperative morbidity (RR: 0.79, 95% CI: 0.58-1.08). In conclusion, the application of ICG in laparoscopic colorectal surgery can effectively reduce the AL, lymph node detection, and hospitalization time. However, more multicenter large-sample randomized controlled trials are required to further confirm its advantages. The meta-analysis was registered in PROSPERO (no. CRD42022288054).
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Affiliation(s)
- Jia Deng
- College of Clinical Medicine, Guizhou University of Traditional Chinese Medicine, Guiyang, China
| | - Wenting Hu
- College of Clinical Medicine, Guizhou University of Traditional Chinese Medicine, Guiyang, China
- College of Pharmacy, Dali University, Dali, China
| | - Yang Li
- College of Pharmacy, Dali University, Dali, China
- Colorectal and Anal Surgery, The First Affiliated Hospital of Guizhou, University of Traditional Chinese Medicine, Guiyang, China
| | - Kai Xiong
- College of Clinical Medicine, Guizhou University of Traditional Chinese Medicine, Guiyang, China
| | - Tinghui Yue
- College of Clinical Medicine, Guizhou University of Traditional Chinese Medicine, Guiyang, China
| | - Xiangquan Lai
- Colorectal and Anal Surgery, The First Affiliated Hospital of Guizhou, University of Traditional Chinese Medicine, Guiyang, China
| | - Tianbao Xiao
- Colorectal and Anal Surgery, The First Affiliated Hospital of Guizhou, University of Traditional Chinese Medicine, Guiyang, China
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Sposito C, Maspero M, Belotti P, Simonotti N, Altomare M, Ciana P, Mazzaferro V. Indocyanine Green Fluorescence-Guided Surgery for Gastrointestinal Tumors: A Systematic Review. ANNALS OF SURGERY OPEN 2022; 3:e190. [PMID: 37601143 PMCID: PMC10431291 DOI: 10.1097/as9.0000000000000190] [Citation(s) in RCA: 14] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/17/2022] [Accepted: 06/28/2022] [Indexed: 11/25/2022] Open
Abstract
Objective To conduct a systematic review of the currently available literature on the use of ICG to guide surgical dissection in gastrointestinal (GI) cancer surgery. Background Real-time indocyanine green (ICG) fluorescence-guided surgery has the potential to enhance surgical outcomes by increasing patient-tailored oncological precision. Methods MEDLINE, PubMed, EMBASE, and Google Scholar were searched for publications on the use of ICG as a contrast agent in GI cancer surgery until December 2020. Perfusion studies were excluded. Quality of the studies was assessed with the Methodological Index for nonrandomized Studies or Jadad scale for randomized controlled trials. A narrative synthesis of the results was provided, with descriptive statistics when appropriate. Results Seventy-eight studies were included. ICG was used for primary tumor and metastases localization, for sentinel lymph node detection, and for lymph flow mapping. The detection rate for primary colorectal and gastric tumors was 100% after preoperative ICG endoscopic injection. For liver lesions, the detection rate after intravenous ICG infusion was 80% and up to 100% for lesions less than 8 mm from the liver surface. The detection rate for sentinel lymph nodes was 89.8% for esophageal, 98.6% for gastric, 87.4% for colorectal, and 83.3% for anal tumors, respectively. In comparative studies, ICG significantly increases the quality of D2 lymphadenectomy in oncological gastrectomy. Conclusion The use of ICG as a guiding tool for dissection in GI surgery is promising. Further evidence from high-quality studies on larger sample sizes is needed to assess whether ICG-guided surgery may become standard of care.
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Affiliation(s)
- Carlo Sposito
- From the General Surgery and Liver Transplantation Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy
- Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy
| | - Marianna Maspero
- From the General Surgery and Liver Transplantation Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy
- University of Milan, Milan, Italy
| | | | | | | | - Paolo Ciana
- Department of Health Sciences, Institute of Pharmacology, University of Milan, Milan, Italy
| | - Vincenzo Mazzaferro
- From the General Surgery and Liver Transplantation Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy
- Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy
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Morales-Conde S, Licardie E, Alarcón I, Balla A. Indocyanine green (ICG) fluorescence guide for the use and indications in general surgery: recommendations based on the descriptive review of the literature and the analysis of experience. Cir Esp 2022; 100:534-554. [PMID: 35700889 DOI: 10.1016/j.cireng.2022.06.023] [Citation(s) in RCA: 14] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/11/2021] [Accepted: 11/26/2021] [Indexed: 06/15/2023]
Abstract
Indocyanine Green is a fluorescent substance visible in near-infrared light. It is useful for the identification of anatomical structures (biliary tract, ureters, parathyroid, thoracic duct), the tissues vascularization (anastomosis in colorectal, esophageal, gastric, bariatric surgery, for plasties and flaps in abdominal wall surgery, liver resection, in strangulated hernias and in intestinal ischemia), for tumor identification (liver, pancreas, adrenal glands, implants of peritoneal carcinomatosis, retroperitoneal tumors and lymphomas) and sentinel node identification and lymphatic mapping in malignant tumors (stomach, breast, colon, rectum, esophagus and skin cancer). The evidence is very encouraging, although standardization of its use and randomized studies with higher number of patients are required to obtain definitive conclusions on its use in general surgery. The aim of this literature review is to provide a guide for the use of ICG fluorescence in general surgery procedures.
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Affiliation(s)
- Salvador Morales-Conde
- Unit of Innovation in Minimally Invasive Surgery, Department of General and Digestive Surgery, University Hospital Virgen del Rocio, University of Sevilla, Sevilla, Spain; Unit of General and Digestive Surgery, Hospital Quironsalud Sagrado Corazón, Sevilla, Spain.
| | - Eugenio Licardie
- Unit of General and Digestive Surgery, Hospital Quironsalud Sagrado Corazón, Sevilla, Spain.
| | - Isaias Alarcón
- Unit of Innovation in Minimally Invasive Surgery, Department of General and Digestive Surgery, University Hospital Virgen del Rocio, University of Sevilla, Sevilla, Spain.
| | - Andrea Balla
- Unit of Innovation in Minimally Invasive Surgery, Department of General and Digestive Surgery, University Hospital Virgen del Rocio, University of Sevilla, Sevilla, Spain; UOC of General and Minimally Invasive Surgery, Hospital "San Paolo", Civitavecchia, Rome, Italy.
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Deng C, Zhang Z, Qi H, Guo Z, Liu Y, Xiao H, Li X. Safety and efficacy of indocyanine green near-infrared fluorescent imaging-guided lymph nodes dissection during radical gastrectomy for gastric cancer: A systematic review and meta-analysis. Front Oncol 2022; 12:917541. [PMID: 36052237 PMCID: PMC9425773 DOI: 10.3389/fonc.2022.917541] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/11/2022] [Accepted: 07/12/2022] [Indexed: 12/29/2022] Open
Abstract
Background Indocyanine green (ICG) fluorescence imaging has been a new surgical navigation technique for gastric cancer. However, its clinical value should still be evaluated further. In this meta-analysis, we investigated the safety and efficacy of ICG near-infrared fluorescent imaging-guided lymph nodes (LNs) dissection during radical gastrectomy. Methods Studies comparing ICG fluorescence imaging with standard care in patients with gastric cancer were systematically searched from PubMed, Embase, Web of Science, and Cochrane Library through August 2021. The current meta-analysis was performed according to the preferred reporting items for systematic review and meta-analysis guidelines. A pooled analysis was performed for the available data regarding the number of LNs dissection, the number of metastatic LNs dissection, other operative outcomes, and postoperative complications. R software version 4.2.0 and Stata 16.0 software were used for the present meta-analysis. Results This analysis included 12 studies with a total of 1365 gastric cancer patients (569 in the ICG group and 796 in the non-ICG group). The number of retrieved LNs in the ICG group was significantly higher (weighted mean difference [WMD]=7.67, 95% confidence intervals [CI]: 4.73 to 10.62, P<0.05) compared to the non-ICG group with moderate heterogeneity (P<0.001, I2 = 70%). The number of metastatic LNs, operative time, and postoperative complications were all comparable and without significant heterogeneity. Additionally, ICG near-infrared fluorescent imaging was associated with reduced intraoperative blood loss (WMD=-10.28, 95% CI: -15.22 to -5.35, P<0.05) with low heterogeneity (P=0.07, I2 = 43%). Conclusions ICG near-infrared fluorescent imaging-guided lymphadenectomy was considered to be safe and effective in gastrectomy. ICG was used to increase the number of LNs harvested while reducing intraoperative blood loss without increasing operative time or postoperative complications. Systematic Review Registration https://www.crd.york.ac.uk/PROSPERO/, identifier CRD42021291863.
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Affiliation(s)
- Chun Deng
- Department of Gastrointestinal Surgery, the Second People’s Hospital of Yibin, Yibin City, China
| | - Zhenyu Zhang
- Department of General Surgery, Shaanxi Provincial People’s Hospital, Xi’an City, China
| | - Hengduo Qi
- Department of General Surgery, Shaanxi Provincial People’s Hospital, Xi’an City, China
| | - Zhi Guo
- Department of General Surgery, Shaanxi Provincial People’s Hospital, Xi’an City, China
| | - Yang Liu
- Department of General Surgery, Shaanxi Provincial People’s Hospital, Xi’an City, China
| | - Haimin Xiao
- Department of General Surgery, Shaanxi Provincial People’s Hospital, Xi’an City, China
| | - Xiaojun Li
- Department of General Surgery, Shaanxi Provincial People’s Hospital, Xi’an City, China
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Yoshida M, Tanaka M, Kitagawa N, Nozawa K, Shinkai M, Goto H, Tanaka Y. Clinicopathological study of surgery for pulmonary metastases of hepatoblastoma with indocyanine green fluorescent imaging. Pediatr Blood Cancer 2022; 69:e29488. [PMID: 34889497 DOI: 10.1002/pbc.29488] [Citation(s) in RCA: 10] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/05/2021] [Revised: 11/05/2021] [Accepted: 11/08/2021] [Indexed: 11/08/2022]
Abstract
BACKGROUND The prognosis of metastatic hepatoblastoma remains poor; to improve it, pulmonary metastasis must be controlled. Indocyanine green (ICG) fluorescent imaging has been used recently for lung metastasectomy. The objective of our study was to clarify the usefulness of ICG imaging for lung metastasectomy of hepatoblastoma using detailed clinicopathological analysis. PROCEDURE Patients with hepatoblastoma who underwent resection of pulmonary metastases with ICG fluorescent imaging were studied using a retrospective analysis of clinical information, a review of their surgical records, and a histological analysis of their metastatic nodules. RESULTS Sixteen patients were enrolled. In total, 61 ICG imaging-guided pulmonary metastasectomies were performed, and 350 ICG-positive and 23 ICG-negative specimens were identified. Tumors were confirmed in 250 of the ICG-positive specimens, including eight nonpalpable nodules, on microscopic examination. ICG-positive and tumor-negative specimens showed histological changes suggesting the regression of a tumor or bloodstream disturbance. CONCLUSIONS Surgical resection is one of the few treatment strategies available to patients with hepatoblastoma with multiple relapses of pulmonary metastasis resistant to chemotherapy. This study demonstrates the high sensitivity of ICG imaging and that thorough metastasectomy can be achieved with ICG imaging. Because a number of false-positive specimens were detected, further optimization of the dose of ICG and the timing of its administration, and establishment of detection of ICG-positive, tumor-negative nodules during surgery are important issues. Several false-negative specimens were also detected, suggesting the presence of ICG-negative metastatic tumors. Palpation during surgery and imaging studies remain essential for detecting metastatic lesions, even in the era of ICG imaging.
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Affiliation(s)
- Misa Yoshida
- Department of Pathology, Kanagawa Children's Medical Center, Mutsukawa, Minami-Ward, Yokohama, Kanagawa, Japan
| | - Mio Tanaka
- Department of Pathology, Kanagawa Children's Medical Center, Mutsukawa, Minami-Ward, Yokohama, Kanagawa, Japan
| | - Norihiko Kitagawa
- Department of Surgery, Kanagawa Children's Medical Center, Mutsukawa, Minami-Ward, Yokohama, Kanagawa, Japan
| | - Kumiko Nozawa
- Department of Radiology, Kanagawa Children's Medical Center, Mutsukawa, Minami-Ward, Yokohama, Kanagawa, Japan
| | - Masato Shinkai
- Department of Surgery, Kanagawa Children's Medical Center, Mutsukawa, Minami-Ward, Yokohama, Kanagawa, Japan
| | - Hiroaki Goto
- Department of Hematology and Oncology, Kanagawa Children's Medical Center, Mutsukawa, Minami-Ward, Yokohama, Kanagawa, Japan
| | - Yukichi Tanaka
- Department of Pathology, Kanagawa Children's Medical Center, Mutsukawa, Minami-Ward, Yokohama, Kanagawa, Japan
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Kim HJ, Choi GS, Park JS, Park SY, Lee SM, Song SH. Stepwise Improvement of Surgical Quality in Robotic Lateral Pelvic Node Dissection: Lessons From 100 Consecutive Patients With Locally Advanced Rectal Cancer. Dis Colon Rectum 2022; 65:599-607. [PMID: 34759242 DOI: 10.1097/dcr.0000000000002329] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/08/2023]
Abstract
BACKGROUND Lateral pelvic node dissection has significant technical difficulty and a high incidence of surgical morbidity. A steep learning curve is anticipated in performing lateral pelvic node dissection. However, no study has previously analyzed the learning curve and surgical skill acquisition for this complex procedure. OBJECTIVES We aimed to evaluate the learning process for performing robotic total mesorectal excision with lateral pelvic node dissection in patients with rectal cancer. DESIGN This is a retrospective analysis of a prospectively collected database. SETTING This study was conducted at a tertiary cancer center. PATIENTS A total of 100 patients who underwent robotic total mesorectal excision with lateral pelvic node dissection between 2011 and 2017 were included. MAIN OUTCOME MEASURES A cumulative sum analysis was calculated based on the number of unilateral retrieved lateral pelvic nodes. Operative time, estimated bloodloss, lateral pelvic node metastatic rate, postoperative morbidities, and local recurrence were also analyzed. RESULTS Cumulative sum modeling suggested 4 learning phases: learning I (33 patients), learning II (19 patients), consolidation (30 patients), and competence (18 patients). In the consolidation and competence phases, we adopted fluorescence imaging and standardized the surgical procedure on the basis of anatomical planes. The competence phase had the greatest number of unilateral retrieved lateral pelvic nodes (12.8 vs 4.9, 8.2, and 10.4; p < 0.001). Urinary complications, including urinary retention and postoperative α-blocker usage, were more frequently observed in learning phase I than in the competence phase (39.4% vs 16.7%, p = 0.034). During the median follow-up of 44.2 months, local recurrence in the pelvic sidewall was observed in 4 patients from learning phase I and in 1 patient from learning phase II. LIMITATIONS This study was limited by its retrospective design. CONCLUSION Completeness of the lateral pelvic node dissection procedure increased with the surgeon's experience and as new imaging systems and surgical technique standardization were implemented. Further studies are warranted to determine the oncologic outcomes associated with each phase. See Video Abstract at http://links.lww.com/DCR/B774. MEJORA GRADUAL DE LA CALIDAD QUIRRGICA EN LA DISECCIN LINFTICA PLVICA LATERAL ROBTICA LECCIONES DE PACIENTES CONSECUTIVOS CON CNCER DE RECTO LOCALMENTE AVANZADO ANTECEDENTES:La disección linfática pélvica lateral tiene una dificultad técnica significativa y una alta incidencia de morbilidad quirúrgica. Se prevé una curva de aprendizaje muy pronunciada al realizar la disección linfática pélvica lateral. Sin embargo, ningún estudio ha analizado previamente la curva de aprendizaje y la adquisición de habilidades quirúrgicas para este procedimiento.OBJETIVOS:Nuestro objetivo fue evaluar el proceso de aprendizaje para realizar la escisión total de mesorrecto robótica con disección linfática pélvica lateral en pacientes con cáncer de recto.DISEÑO:Este es un análisis retrospectivo de una base de datos recopilada prospectivamente.AJUSTE:Este estudio se realizó en un centro oncológico terciario.PACIENTES:Un total de 100 pacientes fueron sometidos a escisión total de mesorrecto robótica con disección linfática pélvica lateral entre 2011 y 2017.PRINCIPALES MEDIDAS DE DESENLACE:Se calculó un análisis de suma acumulativa basado en el número unilateral de ganglios pélvicos laterales recuperados. También se analizaron el tiempo operatorio, la pérdida de sangre estimada, la tasa de metástasis ganglionares pélvicas laterales, las morbilidades postoperatorias y la recidiva local.RESULTADOS:El modelado total acumulativo sugirió cuatro fases de aprendizaje: aprendizaje I (33 pacientes), aprendizaje II (19 pacientes), consolidación (30 pacientes) y competencia (18 pacientes). En las fases de consolidación y competencia, adoptamos imágenes de fluorescencia y estandarizamos el procedimiento quirúrgico basado en planos anatómicos, respectivamente. La fase de competencia tuvo el mayor número de ganglios pélvicos laterales recuperados unilateralmente (12,8 frente a 4,9, 8,2 y 10,4; p < 0,001). Las complicaciones urinarias, incluida la retención urinaria y el uso posoperatorio de bloqueadores beta, se observaron con más frecuencia en la fase de aprendizaje I que en la fase de competencia (39,4% frente a 16,7%, p = 0,034). Durante la mediana de seguimiento de 44,2 meses, se observó una recidiva local en la pared lateral pélvica en cuatro pacientes de la fase de aprendizaje I y en un paciente de la fase de aprendizaje II.LIMITACIONES:Este estudio estuvo limitado por su diseño retrospectivo.CONCLUSIÓNES:La completitud del procedimiento de disección linfática pélvica lateral aumentó con la experiencia del cirujano y a medida que se implementaron nuevos sistemas de imágenes y estandarización de técnicas quirúrgicas. Se necesitan más estudios para determinar los resultados oncológicos asociados con cada fase. Consulte Video Resumen en http://links.lww.com/DCR/B774.
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Affiliation(s)
- Hye Jin Kim
- Colorectal Cancer Center, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, Daegu, Korea
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Guía de uso e indicaciones de la fluorescencia con verde de indocianina (ICG) en cirugía general: recomendaciones basadas en la revisión descriptiva de la literatura y el análisis de la experiencia. Cir Esp 2022. [DOI: 10.1016/j.ciresp.2021.11.018] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/27/2022]
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Numata M, Shiozawa M, Godai T, Kazama K, Okamoto H, Kato A, Katayama Y, Sato S, Sugano N, Kohmura T, Higuchi A, Saito K, Iguchi K, Atsumi Y, Aoyama T, Tamagawa H, Mushiake H, Saeki H, Yukawa N, Taguri M, Sato M, Rino Y. Prediction of lateral lymph node metastasis using OSNA method for mesorectal lymph nodes in low rectal cancer: A prospective study by the Kanagawa Yokohama Colorectal Cancer Study Group (KYCC1801). J Surg Oncol 2021; 125:457-464. [PMID: 34704609 DOI: 10.1002/jso.26730] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/15/2021] [Accepted: 10/19/2021] [Indexed: 12/19/2022]
Abstract
BACKGROUND AND OBJECTIVES Contrary to the Japanese guidelines recommendations regarding lateral lymph node dissection (LatLND) for rectal cancer, its omission is common in clinical practice without reliable omission criteria. Negative pathological mesorectal lymph node metastasis (MesLNM) is reportedly highly correlated with negative pathological lateral lymph node metastasis (p-LatLNM); however, this cannot be used as a criterion because pathological features are revealed postoperatively. Herein, we prospectively evaluated the negative predictive value (NPV) of MesLNM diagnosed via the one-step nucleic acid amplification (OSNA) method for p-LatLNM. METHODS This prospective study was conducted at a single academic study group in Japan. The key eligibility criterion was mid-to-low rectal cancer planned to be treated using mesorectal excision with LatLND. According to the study protocol, the OSNA method was considered useful if the point estimate of the NPV exceeded 95%. RESULTS Preoperative case registration was conducted between 2018 and 2020; 34 patients were registered. Among these, 16 were negative for OSNA-MesLNM, and negative p-LatLNM was confirmed in all cases. The point estimate of the NPV was 100%, with the 95% confidence interval ranging from 79.4% to 100.0%. CONCLUSIONS The OSNA method is useful in selecting patients in whom LatLND can be omitted in real-world clinical practice.
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Affiliation(s)
- Masakatsu Numata
- Department of Surgery, Yokohama City University, Yokohama, Kanagawa, Japan
| | - Manabu Shiozawa
- Department of Gastroenterological Surgery, Kanagawa Cancer Center, Yokohama, Kanagawa, Japan
| | - Teni Godai
- Department of Surgery, Fujisawa Shonandai Hospital, Fujisawa, Kanagawa, Japan
| | - Keisuke Kazama
- Department of Surgery, Yokohama City University, Yokohama, Kanagawa, Japan
| | - Hironao Okamoto
- Department of Gastroenterological Surgery, Kanagawa Cancer Center, Yokohama, Kanagawa, Japan
| | - Aya Kato
- Department of Surgery, Yokohama Minami Kyousai Hospital, Yokohama, Kanagawa, Japan
| | - Yusuke Katayama
- Department of Surgery, Hadano Red Cross Hospital, Hadano, Kanagawa, Japan
| | - Sumito Sato
- Department of Gastroenterological Surgery, Kanagawa Cancer Center, Yokohama, Kanagawa, Japan
| | - Nobuhiro Sugano
- Department of Gastroenterological Surgery, Kanagawa Cancer Center, Yokohama, Kanagawa, Japan
| | - Takashi Kohmura
- Department of Gastroenterological Surgery, Kanagawa Cancer Center, Yokohama, Kanagawa, Japan
| | - Akio Higuchi
- Department of Surgery, Yokohama Minami Kyousai Hospital, Yokohama, Kanagawa, Japan
| | - Kentaro Saito
- Department of Surgery, Yokohama City University, Yokohama, Kanagawa, Japan
| | - Kenta Iguchi
- Department of Gastroenterological Surgery, Kanagawa Cancer Center, Yokohama, Kanagawa, Japan
| | - Yosuke Atsumi
- Department of Surgery, Yokohama City University, Yokohama, Kanagawa, Japan
| | - Toru Aoyama
- Department of Surgery, Yokohama City University, Yokohama, Kanagawa, Japan
| | - Hiroshi Tamagawa
- Department of Surgery, Yokohama City University, Yokohama, Kanagawa, Japan
| | - Hiroyuki Mushiake
- Department of Surgery, Saiseikai Yokohama Nanbu Hospital, Yokohama, Kanagawa, Japan
| | - Hiroyuki Saeki
- Department of Surgery, Yokohama Minami Kyousai Hospital, Yokohama, Kanagawa, Japan
| | - Norio Yukawa
- Department of Surgery, Yokohama City University, Yokohama, Kanagawa, Japan
| | - Masataka Taguri
- Department of Biostatistics, Yokohama City University, Yokohama, Kanagawa, Japan
| | - Maho Sato
- Department of Gastroenterological Surgery, Kanagawa Cancer Center, Yokohama, Kanagawa, Japan
| | - Yasushi Rino
- Department of Surgery, Yokohama City University, Yokohama, Kanagawa, Japan
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23
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Peltrini R, Podda M, Castiglioni S, Di Nuzzo MM, D'Ambra M, Lionetti R, Sodo M, Luglio G, Mucilli F, Di Saverio S, Bracale U, Corcione F. Intraoperative use of indocyanine green fluorescence imaging in rectal cancer surgery: The state of the art. World J Gastroenterol 2021; 27:6374-6386. [PMID: 34720528 PMCID: PMC8517789 DOI: 10.3748/wjg.v27.i38.6374] [Citation(s) in RCA: 29] [Impact Index Per Article: 7.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/18/2021] [Revised: 06/30/2021] [Accepted: 08/18/2021] [Indexed: 02/06/2023] Open
Abstract
Indocyanine green (ICG) fluorescence imaging is widely used in abdominal surgery. The implementation of minimally invasive rectal surgery using new methods like robotics or a transanal approach required improvement of optical systems. In that setting, ICG fluorescence optimizes intraoperative vision of anatomical structures by improving blood and lymphatic flow. The purpose of this review was to summarize all potential applications of this upcoming technology in rectal cancer surgery. Each type of use has been separately addressed and the evidence was investigated. During rectal resection, ICG fluorescence angiography is mainly used to evaluate the perfusion of the colonic stump in order to reduce the risk of anastomotic leaks. In addition, ICG fluorescence imaging allows easy visualization of organs such as the ureter or urethra to protect them from injury. This intraoperative technology is a valuable tool for conducting lymph node dissection along the iliac lymphatic chain or to better identifying the rectal dissection planes when a transanal approach is performed. This is an overview of the applications of ICG fluorescence imaging in current surgical practice and a synthesis of the results obtained from the literature. Although further studies are need to investigate the real clinical benefits, these findings may enhance use of ICG fluorescence in current clinical practice and stimulate future research on new applications.
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Affiliation(s)
- Roberto Peltrini
- Department of Public Health, University of Naples Federico II, Napoli 80131, Italy
| | - Mauro Podda
- Department of Emergency Surgery, Cagliari University Hospital "Duilio Casula", Azienda Ospedaliero-Universitaria di Cagliari, Cagliari 09100, Italy
| | - Simone Castiglioni
- Department of Medical, Oral and Biotechnological Sciences, University G. D’Annunzio Chieti-Pescara, Pescara 65100, Italy
| | | | - Michele D'Ambra
- Department of Public Health, University of Naples Federico II, Napoli 80131, Italy
| | - Ruggero Lionetti
- Department of Public Health, University of Naples Federico II, Napoli 80131, Italy
| | - Maurizio Sodo
- Department of Public Health, University of Naples Federico II, Napoli 80131, Italy
| | - Gaetano Luglio
- Department of Public Health, University of Naples Federico II, Napoli 80131, Italy
| | - Felice Mucilli
- Department of Medical, Oral and Biotechnological Sciences, University G. D’Annunzio Chieti-Pescara, Pescara 65100, Italy
| | - Salomone Di Saverio
- Department of General Surgery, University of Insubria, ASST Sette Laghi, Varese 21100, Italy
| | - Umberto Bracale
- Department of Public Health, University of Naples Federico II, Napoli 80131, Italy
| | - Francesco Corcione
- Department of Public Health, University of Naples Federico II, Napoli 80131, Italy
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24
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Martínez-López E, Martínez-Pérez A, Navarro-Martínez S, Sebastián-Tomás JC, de'Angelis N, García-Granero E. Real-time fluorescence image-guided gastrointestinal oncologic surgery: Towards a new era. World J Gastrointest Oncol 2021; 13:1029-1042. [PMID: 34616510 PMCID: PMC8465438 DOI: 10.4251/wjgo.v13.i9.1029] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/22/2021] [Revised: 06/14/2021] [Accepted: 07/27/2021] [Indexed: 02/06/2023] Open
Abstract
Technological improvements are crucial in the evolution of surgery. Real-time fluorescence-guided surgery (FGS) has spread worldwide, mainly because of its usefulness during the intraoperative decision-making processes. The success of any gastrointestinal oncologic resection is based on the anatomical identification of the primary tumor and its regional lymph nodes. FGS allows also to evaluate the blood perfusion at the gastrointestinal stumps after colorectal or esophageal resections. Therefore, a reduction on the anastomotic leak rates has been postulated as one of the foreseeable benefits provided by the use of FGS in these procedures. Although the use of fluorescence in lymph node detection was initially described in breast cancer surgery, the technique is currently applied in gastric or splenic flexure cancers, as they both present complex and variable lymphatic drainages. FGS allows also to perform intraoperative lymphograms or sentinel lymph node biopsies. New applications of FGS are being developed to assist in the detection of peritoneal metastases or in the evaluation of the tumor resection margins. The present review aims to provide a general overview of the current status of real-time FGS in gastrointestinal oncologic surgery. We put a special focus on the different applications of FGS, discussing the main findings and limitations found in the contemporary literature and also the promising near future applications.
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Affiliation(s)
- Elías Martínez-López
- Department of Surgery, University of Valencia, Valencia 46010, Spain
- Department of General and Digestive Surgery, Hospital Universitario Doctor Peset, Valencia 46017, Spain
| | - Aleix Martínez-Pérez
- Faculty of Health Sciences, Valencian International University, Valencia 46002, Spain
- Minimally Invasive and Robotic Digestive Surgery Unit, Miulli Hospital, Acquaviva delle Fonti 70021, Italy
| | - Sergio Navarro-Martínez
- Department of General and Digestive Surgery, Hospital Universitario Doctor Peset, Valencia 46017, Spain
| | - Juan Carlos Sebastián-Tomás
- Department of Surgery, University of Valencia, Valencia 46010, Spain
- Department of General and Digestive Surgery, Hospital Universitario Doctor Peset, Valencia 46017, Spain
| | - Nicola de'Angelis
- Minimally Invasive and Robotic Digestive Surgery Unit, Miulli Hospital, Acquaviva delle Fonti 70021, Italy
| | - Eduardo García-Granero
- Department of Surgery, University of Valencia, Valencia 46010, Spain
- Department of General and Digestive Surgery, Hospital Universitario y Politécnico La Fe, Valencia 46026, Spain
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25
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Yasui M, Ohue M, Noura S, Miyoshi N, Takahashi Y, Matsuda C, Nishimura J, Haraguchi N, Ushigome H, Nakai N, Fujino S, Sugimura K, Wada H, Takahashi H, Omori T, Miyata H. Exploratory analysis of lateral pelvic sentinel lymph node status for optimal management of laparoscopic lateral lymph node dissection in advanced lower rectal cancer without suspected lateral lymph node metastasis. BMC Cancer 2021; 21:911. [PMID: 34380428 PMCID: PMC8356457 DOI: 10.1186/s12885-021-08480-6] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/16/2021] [Accepted: 06/10/2021] [Indexed: 03/05/2023] Open
Abstract
BACKGROUND Total mesorectal excision (TME) and lateral lymph node dissection (LLND) without radiotherapy (RT) are standard treatment for lower cT3/4 rectal cancers in Eastern countries. In comparative studies, both TME + LLND and RT + TME yield good local control. Although Japanese guidelines recommend LLND for locally advanced rectal cancers below the peritoneal reflection, LLND dissection of clinically negative lateral pelvic lymph nodes (LPLN) is controversial, and laparoscopic TME + LLND is technically challenging and time-consuming. New optical instruments for laparoscopy allow easy perioperative sentinel lymph node (SLN) identification using ICG. The SLN concept may facilitate accurate diagnosis of LPLN involvement, and thus reduce LLND in laparoscopic rectal cancer surgery. Here we investigated lateral pelvic SLN navigation surgery for SLN detection during laparoscopic rectal cancer surgery. METHODS This study included 21 patients with clinical StageII/III lower rectal cancer without LPLN enlargement, who underwent curative laparoscopic surgery. All patients underwent TME, followed by lateral SLN identification and biopsy using ICG, and then laparoscopic LLND. ICG fluorescence imaging was conducted using the laparoscopic near-infrared camera system. RESULTS Lateral SLNs were successfully identified in 16 (76.2%) of the 21 patients. Among the 15 patients without SLN tumor metastasis, the dissected lateral non-SLNs were all negative. CONCLUSIONS A lack of metastasis in the lateral pelvic SLN seems to reflect a lack of metastases to all lateral LNs. Our present results suggest that this laparoscopic ICG-guided SLN strategy may be a low-risk and time-saving method to prevent laparoscopic LLND in cases with negative lateral pelvic lymph nodes.
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Affiliation(s)
- Masayoshi Yasui
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan.
| | - Masayuki Ohue
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Shingo Noura
- Department of Surgery, Toyonaka Municipal Hospital, Osaka, Japan
| | - Norikatsu Miyoshi
- Department of Gastroenterological Surgery, Osaka University, Osaka, Japan
| | | | - Chu Matsuda
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Junichi Nishimura
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Naotsugu Haraguchi
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Hajime Ushigome
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Nozomu Nakai
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Shiki Fujino
- Department of Gastroenterological Surgery, Osaka University, Osaka, Japan
| | - Keijiro Sugimura
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Hiroshi Wada
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Hidenori Takahashi
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Takeshi Omori
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
| | - Hiroshi Miyata
- Department of Gastroenterological Surgery, Osaka International Cancer Institute, Otemae 3-1-69, Chuo-ku, Osaka City, Osaka, Japan
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26
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Son GM, Ahn HM, Lee IY, Ha GW. Multifunctional Indocyanine Green Applications for Fluorescence-Guided Laparoscopic Colorectal Surgery. Ann Coloproctol 2021; 37:133-140. [PMID: 34102813 PMCID: PMC8273708 DOI: 10.3393/ac.2021.05.07] [Citation(s) in RCA: 34] [Impact Index Per Article: 8.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/22/2021] [Accepted: 05/07/2021] [Indexed: 12/17/2022] Open
Abstract
Indocyanine green (ICG) could be applied for multiple functions such as fluorescent tumor localization, fluorescence lymph node mapping (FLNM), and intraoperative angiography in colorectal cancer surgery. With the near-infrared (NIR) systems, colonoscopic ICG tattooing can be used to define the early colorectal cancer that cannot be easily distinguished through the serosal surface. The lymphatic pathways can be visualized under the NIR system when ICG is injected through the submucosal or subserosal layer around the tumor. Intraoperative ICG angiography can be applied to find a favorable perfusion segment before the colon transection. Although all fluorescence functions are considered essential steps in image-guided surgery, it is difficult to perform multifunctional ICG applications in a single surgical procedure at once because complex protocols could interfere with each other. Therefore, we review the multifunctional ICG applications for fluorescent tumor localization, FLNM, and ICG angiography. We also discuss the optimal protocol for fluorescence-guided colorectal surgery.
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Affiliation(s)
- Gyung Mo Son
- Department of Surgery, Pusan National University Yangsan Hospital, Yangsan, Korea.,Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea.,Medical Research Center, Pusan National University School of Medicine, Yangsan, Korea
| | - Hong-Min Ahn
- Department of Surgery, Pusan National University Yangsan Hospital, Yangsan, Korea
| | - In Young Lee
- Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea.,Medical Research Center, Pusan National University School of Medicine, Yangsan, Korea
| | - Gi Won Ha
- Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, Korea
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27
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Matsuki R, Sugiyama M, Kogure M, Yokoyama M, Nakazato T, Suzuki Y, Mori T, Abe N, Sakamoto Y. Optimal Lymphadenectomy of the Mesopancreas Based on Fluorescence Imaging During Pancreaticoduodenectomy. J Gastrointest Surg 2021; 25:1241-1246. [PMID: 32462494 DOI: 10.1007/s11605-020-04619-1] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/13/2020] [Accepted: 04/19/2020] [Indexed: 01/31/2023]
Abstract
BACKGROUND Excision of the mesopancreas with lymphadenectomy is an important component of pancreatoduodenectomy. However, the optimal extent of lymphadenectomy remains unclear. Furthermore, accurate description of the mesopancreatic lymphatic pathways is difficult, probably because of the complex anatomy. Intestinal derotation simplifies the anatomy and facilitates both examination of lymphatic flow and the surgical procedure. The aim of this study was to evaluate lymphatic flow in the mesopancreas using indocyanine green fluorescence imaging with an intestinal derotation technique, and to clarify the optimal extent of mesopancreas excision and lymphadenectomy in pancreatoduodenectomy. METHODS Indocyanine green solution (2.5 × 10-3 mg) was injected into the pancreatic head parenchyma. After intestinal derotation, the spread of indocyanine green was observed using near-infrared imaging. RESULTS Participants comprised 10 patients who underwent pancreatoduodenectomy for periampullary neoplasms. With indocyanine green fluorescence imaging, 9 of the 10 patients showed lymphatic flow from the pancreatic head to the superior mesenteric artery via the inferior pancreaticoduodenal artery and first jejunal artery (but not via the second and more distant arteries), with eventual drainage into the paraaortic region. CONCLUSIONS Lymphatic pathways from the pancreatic head were connected to the superior mesenteric artery via the inferior pancreaticoduodenal artery and first jejunal artery. Excision of the mesopancreas with the inferior pancreaticoduodenal artery and first jejunal artery while preserving the second or more distant arteries appears optimal in pancreatoduodenectomy for periampullary malignancies.
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Affiliation(s)
- Ryota Matsuki
- Department of Surgery, Kyorin University, School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan
| | - Masanori Sugiyama
- Tokyo Rosai Hospital, 4-13-21, Ohmori-Minami, Ohta-ku, Tokyo, 143-0013, Japan
| | - Masaharu Kogure
- Department of Surgery, Kyorin University, School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan
| | - Masaaki Yokoyama
- Kosei Hospital, 2-25-1 Wada, Suginami-ku, Tokyo, 166-0012, Japan
| | - Tetsuya Nakazato
- Department of Surgery, Kyorin University, School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan
| | - Yutaka Suzuki
- Department of Surgery, Kyorin University, School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan
| | - Toshiyuki Mori
- Department of Surgery, Kyorin University, School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan
| | - Nobutsugu Abe
- Department of Surgery, Kyorin University, School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan
| | - Yoshihiro Sakamoto
- Department of Surgery, Kyorin University, School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan.
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28
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Ahn HM, Son GM, Lee IY, Shin DH, Kim TK, Park SB, Kim HW. Optimal ICG dosage of preoperative colonoscopic tattooing for fluorescence-guided laparoscopic colorectal surgery. Surg Endosc 2021; 36:1152-1163. [PMID: 33638107 PMCID: PMC8758609 DOI: 10.1007/s00464-021-08382-5] [Citation(s) in RCA: 27] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/12/2020] [Accepted: 02/09/2021] [Indexed: 02/06/2023]
Abstract
Background Indocyanine green (ICG) is a multifunctional dye used in tumor localization, tissue perfusion, and lymph node (LN) mapping during fluorescence-guided laparoscopic colorectal surgery. Purpose This study aimed to establish the optimal protocol for preoperative endoscopic submucosal ICG injection to perform fluorescence lymph node mapping (FLNM), along with undisturbed fluorescent tumor localization and ICG angiography during a single surgery. Methods Colorectal cancer patients (n = 192) were enrolled from May 2017 to December 2019. Colonoscopic submucosal ICG injection was performed 12 to 18 h before surgery. ICG injection protocols were modified based on the total injected ICG (mg) and tattooing site number. The concentrations of ICG were gradually decreased from the standard dose (2.5 mg/ml) to the minimum dose (0.2 mg/ml). Successful FLNM (FLNM-s) was defined as distinct fluorescent LNs observed under NIR camera. The patient’s age, sex, body mass index (BMI), stage, cancer location, obstruction, and laboratory findings were compared between the FLNM-s and failed FLNM (FLNM-f) groups to identify clinical and pathological factors that affect FLNM. Results In the ICG dose section of 0.5 to 1 mg, the success rate was highest within all functions including FLNM, fluorescent tumor localization, and ICG angiography. FLNM-s was related to ICG dose (0.5–1 mg), multiple submucosal injections, location of cancer, camera light source, and lower BMI. In the multivariate analysis, camera light source, non-obesity, and multiple injections were independent factors for FLNM-s). The mean total number of harvested LNs was significantly higher in the FLNM-s group than that in the FLNM-f group (p < 0.001). The number of metastatic lymph nodes was comparable between the two groups (p = 0.859). Conclusions Preoperative, endoscopic submucosal ICG injection with dose range 0.5 to 1 mg would be optimal protocol for multifunctional ICG applications during fluorescence-guided laparoscopic colorectal surgery.
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Affiliation(s)
- Hong-Min Ahn
- Department of Surgery, Pusan National University Yangsan Hospital, 50612, 20, Geumo-ro, Mulgeum-eup, Yangsan-si, Gyeongsangnam-do, Yangsan, Korea.,Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea
| | - Gyung Mo Son
- Department of Surgery, Pusan National University Yangsan Hospital, 50612, 20, Geumo-ro, Mulgeum-eup, Yangsan-si, Gyeongsangnam-do, Yangsan, Korea. .,Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea. .,Medical Research Center, School of Medicine, Pusan National University, Yangsan, Korea.
| | - In Young Lee
- Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea.,Medical Research Center, School of Medicine, Pusan National University, Yangsan, Korea
| | - Dong-Hoon Shin
- Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea.,Department of Pathology, School of Medicine, Pusan National University, Yangsan, Korea
| | - Tae Kyun Kim
- Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea.,Department of Anesthesia and Pain Medicine, Pusan National University, Yangsan, Korea
| | - Su Bum Park
- Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea.,Department of Internal Medicine, School of Medicine, Pusan National University, Yangsan, Korea
| | - Hyung Wook Kim
- Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea.,Department of Internal Medicine, School of Medicine, Pusan National University, Yangsan, Korea
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29
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Elhusseini M, Aly EH. Lateral pelvic lymph node dissection in the management of locally advanced low rectal cancer: Summary of the current evidence. Surg Oncol 2020; 35:418-425. [PMID: 33038847 DOI: 10.1016/j.suronc.2020.09.021] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/11/2020] [Revised: 08/23/2020] [Accepted: 09/27/2020] [Indexed: 02/07/2023]
Abstract
Lateral pelvic lymph nodes (LPLN) are a major site for local recurrence following curative resection for low locally advanced rectal cancer. Ongoing advances in imaging techniques have improved predicting LPLN metastasis (LPLNM) during pre-operative staging. However, there is ongoing debate on optimal management of this subgroup of patients with variation between guidance of different societies. In Japan, LPLNM is considered as local disease and addressed by lateral pelvic node dissection (LPLND) in addition to total mesorectal excision (TME). However, in the west, LPLNM is considered as metastatic disease and those patients are offered neoadjuvant chemoradiotherapy (nCRT) followed by TME surgery. The potential surgical risks and morbidity associated with LPLND as well as the uncertainty of the oncological outcome have raised the concern that patients with locally advanced low rectal cancer with LPLNM could be over or under-treated. A comprehensive review of literature was performed, summarizing the current evidence on available modalities for predicting LPLNM, the role of LPLND in the management of advanced low rectal cancer and the available surgical approaches with their impact on surgical and oncological outcomes. LPLND is associated with increased operative time, blood loss and post-operative morbidity. The potential benefits for local disease control and survival still awaits high quality studies. There has been increasing number of reports of the use minimally invasive approaches in LPLND in an attempt to reduce post-operative complications. There is need for high quality evidence to define the role of LPLND in management of patients with advanced low rectal cancer.
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Affiliation(s)
- Mootaz Elhusseini
- University of Aberdeen, UK; Aberdeen Royal Infirmary, Department of Surgery, Surgical Admin Block, Yellow Zone, Level Foresterhill, Aberdeen, Scotland, AB25 2ZN, UK
| | - Emad H Aly
- University of Aberdeen, UK; Aberdeen Royal Infirmary, Department of Surgery, Surgical Admin Block, Yellow Zone, Level Foresterhill, Aberdeen, Scotland, AB25 2ZN, UK.
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30
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Indocyanine Green-Enhanced Colorectal Surgery-between Being Superfluous and Being a Game-Changer. Diagnostics (Basel) 2020; 10:diagnostics10100742. [PMID: 32987841 PMCID: PMC7600504 DOI: 10.3390/diagnostics10100742] [Citation(s) in RCA: 22] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/01/2020] [Revised: 09/10/2020] [Accepted: 09/22/2020] [Indexed: 02/06/2023] Open
Abstract
Nowadays, surgical innovations incorporate new technological conquests and must be validated by evidence-based medicine. The use of augmented reality-assisted indocyanine green (ICG) fluorescence has generated a myriad of intraoperative applications such as demonstration of key anatomical landmarks, sentinel lymph nodes, and real-time assessment of local blood flow. This paper presents a systematic review of the clinical evidence regarding the applications of ICG near-infrared (NIR) fluorescence in colorectal surgery. After we removed duplicate publications and screened for eligibility, a total of 36 articles were evaluated: 23 on perfusion assessment, 10 on lymph node mapping, and 3 on intraoperative identification of ureters. Lack of homogenous studies, low statistical power, and confounding evidence were found to be common amongst publications supporting the use of ICG in colorectal surgery, raising concerns over this seductive technique's cost efficiency and redundancy. The compiled data showed that ICG NIR fluorescence may be a game-changer in particular situations, as proven for low colorectal anastomosis or lateral pelvic lymph node dissection, but it remains controversial for routine use and sentinel lymph node assessment. Further randomized studies are needed to confirm these conclusions. Future research directions include tumor-targeted fluorescence imaging and digital software for quantitative evaluation of fluorescence.
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Liberale G, Vankerckhove S, Bouazza F, Gomez Galdon M, Larsimont D, Moreau M, Bourgeois P, Donckier V. Systemic Sentinel Lymph Node Detection Using Fluorescence Imaging After Indocyanine Green Intravenous Injection in Colorectal Cancer: Protocol for a Feasibility Study. JMIR Res Protoc 2020; 9:e17976. [PMID: 32554370 PMCID: PMC7455862 DOI: 10.2196/17976] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/26/2020] [Revised: 06/04/2020] [Accepted: 06/15/2020] [Indexed: 11/15/2022] Open
Abstract
Background Nodal staging is a major concern in colorectal cancer as it is an important prognostic factor. Several techniques that could potentially improve patient treatment and prognosis have been developed to increase the accuracy of nodal staging. Sentinel lymph node detection has been shown to accurately reflect nodal status in various tumors and has become the standard procedure in nodal staging of breast cancer and melanoma. However, in colorectal cancer, sentinel lymph node detection techniques are still controversial as the sensitivity reported in the literature varies from one study to another. Recently, indocyanine green fluorescence–guided surgery has been reported to be a useful technique for detection of macroscopic and microscopic metastatic deposits in lymph nodes after intravenous administration of indocyanine green dye. However, no studies have focused on the potential role of sentinel lymph node detection after systemic administration of indocyanine green dye, so-called systemic sentinel lymph nodes, or on the correspondence between the identification of the sentinel lymph node by standard local injection techniques and the detection of fluorescent lymph nodes with this new approach. Objective The aim of this protocol is to validate the concept of sentinel lymph nodes identified by fluorescence imaging after intravenous injection of indocyanine green dye and to compare the sentinel lymph nodes identified by fluorescence imaging with sentinel lymph nodes detected by the standard blue dye technique. Methods This study (SeLyNoFI; Sentinel Lymph Nodes Fluorescence Imaging) is a diagnostic, single-arm, open-label feasibility study, including patients with colorectal adenocarcinoma with or without metastatic disease who are admitted for elective colorectal resection of the primary tumor. This study evaluates the feasibility of a new approach for improving the accuracy of nodal staging using fluorescence imaging after intravenous administration of indocyanine green dye. Sensitivity, positive predictive value, and accuracy of the classical blue dye technique and of the investigatory fluorescence imaging technique will be calculated. Translational research will be proposed, if applicable. Results As of June 2020, this study has been registered. Submission for ethical review is planned for September 2020. Conclusions The potential correlation between the two different approaches to detect sentinel lymph nodes offers new strategies for improving the accuracy of nodal staging in colorectal cancer. This new concept of the systemic sentinel lymph node and a greater understanding of the interactions between systemic sentinel lymph nodes and standard sentinel lymph nodes may provide important information regarding the underlying mechanism of primary tumor lymphatic drainage. The enhanced permeability and retention effect can also play a role in the fluorescence of systemic sentinel lymph nodes, especially if these lymph nodes are inflamed. In this case, we can even imagine that this new technique will highlight more instances of lymph node–positive colorectal cancer. International Registered Report Identifier (IRRID) PRR1-10.2196/17976
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Affiliation(s)
- Gabriel Liberale
- Institut Jules Bordet, Belgian Comprehensive Cancer Center, Université Libre de Bruxelles (ULB), BE 0257.981.101., Brussels, Belgium
| | - Sophie Vankerckhove
- Institut Jules Bordet, Belgian Comprehensive Cancer Center, Université Libre de Bruxelles (ULB), BE 0257.981.101., Brussels, Belgium
| | - Fikri Bouazza
- Institut Jules Bordet, Belgian Comprehensive Cancer Center, Université Libre de Bruxelles (ULB), BE 0257.981.101., Brussels, Belgium
| | - Maria Gomez Galdon
- Institut Jules Bordet, Belgian Comprehensive Cancer Center, Université Libre de Bruxelles (ULB), BE 0257.981.101., Brussels, Belgium
| | - Denis Larsimont
- Institut Jules Bordet, Belgian Comprehensive Cancer Center, Université Libre de Bruxelles (ULB), BE 0257.981.101., Brussels, Belgium
| | - Michel Moreau
- Institut Jules Bordet, Belgian Comprehensive Cancer Center, Université Libre de Bruxelles (ULB), BE 0257.981.101., Brussels, Belgium
| | - Pierre Bourgeois
- Institut Jules Bordet, Belgian Comprehensive Cancer Center, Université Libre de Bruxelles (ULB), BE 0257.981.101., Brussels, Belgium
| | - Vincent Donckier
- Institut Jules Bordet, Belgian Comprehensive Cancer Center, Université Libre de Bruxelles (ULB), BE 0257.981.101., Brussels, Belgium
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The Utility of Indocyanine Green Angiography in the Assessment of Perfusion of Gastric Conduit and Proximal Esophageal Stump Against Visual Assessment in Patients Undergoing Esophagectomy: a Prospective Study. Indian J Surg Oncol 2020; 11:684-691. [PMID: 33281408 DOI: 10.1007/s13193-020-01085-8] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/15/2020] [Accepted: 04/28/2020] [Indexed: 01/28/2023] Open
Abstract
Post esophagectomy anastomotic leakage is a crucial factor in determining morbidity and mortality. Good vascularity of the gastric conduit is essential to avoid this complication. This prospective study compares the utility of intraoperative indocyanine green (ICG) fluorescence angiography and visual assessment in assessing the vascularity of gastric conduit and proximal esophageal stump in patients undergoing esophagectomy. Thirteen consecutive patients who underwent esophagectomy for carcinoma middle, lower third esophagus or gastro-esophageal junction from August 2019 to September 2019 were included. Three patients underwent laparoscopic-assisted transhiatal esophagectomy, ten thoraco-laparoscopic-assisted esophagectomy. Reconstruction was done by gastric pull-up via posterior mediastinal route. All patients underwent assessment of perfusion of gastric conduit and proximal esophageal stump by ICG angiography and by visual assessment based on inspection of the color, the palpation of warmth, pulse, and bleeding from the edges. Visual assessment revealed the tip of the gastric conduit was dusky and ischemic in 11 patients, pink and well perfused in two. ICG fluorescence imaging showed inadequate perfusion at the tip of conduit in 12 patients, adequate in one, overall requiring revision in 12 cases. There was a discrepancy in one patient where visual inspection showed adequate perfusion, but ICG disclosed poor vascularity requiring revision of the conduit's tip. Resection of the devitalized portion of the proximal esophageal stump was needed in 5 patients both by visual and by ICG assessment. The median time to appearance of blush from the time of injection of dye was 15 s (10 to 23 s). In all the cases, the pattern of blush was simultaneous, with the concurrent appearance of ICG blush in the gastric conduit and gastro-epiploic arcade. No anastomotic leaks were noted. Visual inspection of the gastric conduit vascularity can underestimate perfusion and hence can compromise resection of the devitalized part. ICG fluorescence imaging is an accurate and promising means to ascertain the vascularity of gastric conduit during an esophagectomy. But its utility needs to be validated in randomized trials.
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Higashijima J, Shimada M, Yoshikawa K, Miyatani T, Tokunaga T, Nishi M, Kashihara H, Takasu C. Usefulness of blood flow evaluation by indocyanine green fluorescence system in laparoscopic anterior resection. THE JOURNAL OF MEDICAL INVESTIGATION 2019; 66:65-69. [PMID: 31064957 DOI: 10.2152/jmi.66.65] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/14/2022]
Abstract
BACKGROUND One of the major cause of anastomotic leakage (AL) in anterior resection of the rectum is insufficient blood flow of the remnant colon. The indocyanine green fluorescence system (ICG-FS) can visualize the blood flow of organs intra-operatively. The aim of this study is to investigate the usefulness of ICG-FS for evaluating the blood flow of the remnant colon in laparoscopic anterior resection. MATERIALS AND METHODS Rectal cancer patients (n=24) who underwent laparoscopic anterior resection were included in this study. After resection of the rectum, 7.5mg of ICG was administered intravenously, and the blood flow of the oral stump was evaluated by the ICG-FS. The relationship between the fluorescence time (FT) of the oral stump and AL was investigated retrospectively. RESULT Two of twenty-four patients (8.3%) suffered AL. The FT of these two cases were over 60 seconds. In the case with the FT was over 80 seconds, we performed additional resection of the late fluorescence portion of the remnant colon and could avoid AL. In patients whose FT was under 60 seconds, no patients suffered AL. CONCLUSION ICG-FS may be useful for evaluating the blood flow of the remnant colon to avoid AL in laparoscopic anterior resection. J. Med. Invest. 66 : 65-69, February, 2019.
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Affiliation(s)
- Jun Higashijima
- Department of Surgery, Institute of Health Biosciences, the University of Tokushima, Japan
| | - Mitsuo Shimada
- Department of Surgery, Institute of Health Biosciences, the University of Tokushima, Japan
| | - Kozo Yoshikawa
- Department of Surgery, Institute of Health Biosciences, the University of Tokushima, Japan
| | - Tomohiko Miyatani
- Department of Surgery, Institute of Health Biosciences, the University of Tokushima, Japan
| | - Takuya Tokunaga
- Department of Surgery, Institute of Health Biosciences, the University of Tokushima, Japan
| | - Masaaki Nishi
- Department of Surgery, Institute of Health Biosciences, the University of Tokushima, Japan
| | - Hideya Kashihara
- Department of Surgery, Institute of Health Biosciences, the University of Tokushima, Japan
| | - Chie Takasu
- Department of Surgery, Institute of Health Biosciences, the University of Tokushima, Japan
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Performance of Indocyanine green for sentinel lymph node mapping and lymph node metastasis in colorectal cancer: a diagnostic test accuracy meta-analysis. Surg Endosc 2019; 34:1035-1047. [PMID: 31754853 DOI: 10.1007/s00464-019-07274-z] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/15/2019] [Accepted: 11/12/2019] [Indexed: 12/12/2022]
Abstract
BACKGROUND Indocyanine green has been widely employed as a secure and easy technique for sentinel lymph node mapping in different types of cancer. Nonetheless, the usage of Indocyanine green has not been fully implemented due to the heterogeneous results found in published studies. Thus, the objective of this meta-analysis is to evaluate the overall performance of Indocyanine green for sentinel lymph node mapping and node metastasis in patients undergoing colorectal cancer surgery. METHODS An extensive systematic search was performed to identify relevant studies in English and Spanish with no time limit restrictions. For the meta-analysis, a hierarchical summary receiver operating characteristic curve (HSROCs) was constructed, and quantitative data synthesis was performed using random effects models. Specificity, sensitivity, positive, and negative likelihood ratios were obtained from the corresponding HSROC. Between-study heterogeneity was visually evaluated using Galbraith plot, and publication bias was quantified using Deeks' method. RESULTS A total of 11 studies were included for analysis. The pooled detection rate for sentinel lymph node mapping was 91% (80-98%). Covariates significantly influencing the pooled detection rate were having colon cancer (estimate: 1.3001; 1.114 to 1.486; p < 0.001) and the usage of a laparoscopic approach (estimate: 1.3495; 1.1029 to 1.5961; p < 0.001). The performance of Indocyanine green for the detection of metastatic lymph nodes yielded an area under the roc curve of 66.5%, sensitivity of 64.3% (51-76%), and specificity of 65% (36-85%). CONCLUSIONS Indocyanine green for the detection of sentinel lymph node mapping demonstrates better accuracy when used in colonic cancer and by a laparoscopic approach. Nevertheless, its overall performance for the detection of lymph node metastasis is poor.
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Picchetto A, Seeliger B, La Rocca S, Barberio M, D'Ambrosio G, Marescaux J, Diana M. [Fluorescence-guided detection of lymph node metastases of gastrointestinal tumors]. Chirurg 2019; 90:891-898. [PMID: 31552436 DOI: 10.1007/s00104-019-01039-z] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/19/2022]
Abstract
A correct lymph node (LN) staging is essential in oncological surgery. Indocyanine green (ICG) near-infrared fluorescence (NIRF) guided sentinel lymph node (SLN) navigation is a relatively novel technique. The aim of this review is to analyze the impact of ICG-NIRF on identification of LN metastases of gastrointestinal tumors. The Scopus and PubMed/MEDLINE literature databases were searched and 20 studies were included. The ICG-NIRF navigation of LN has been shown to enable and improve LN detection in gastrointestinal tumors; however, the mean detection, sensitivity, accuracy and false negative rates show substantial variation. This could be due to both the heterogeneous techniques applied and to the low retention of ICG by lymph nodes. Fluorescence imaging to identify LN drainage is a promising tool to improve oncological outcomes. Nonetheless, the technique requires further development in terms of hardware, software and fluorophores, which are currently being investigated.
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Affiliation(s)
- Andrea Picchetto
- General and Colorectal Surgery Division, Department of Cardiothoracic, Vascular Surgery and Organ Transplantation, Policlinico Umberto I University Hospital, Sapienza University of Rome, Viale del Policlinico 155, Rom, Italien.
| | - Barbara Seeliger
- Institute of Image-Guided Surgery, IHU-Strasbourg, Straßburg, Frankreich
- Research Institute against Cancer of the Digestive System, IRCAD, Straßburg, Frankreich
- Kliniken Essen-Mitte, Essen, Deutschland
| | - Stefania La Rocca
- General and Colorectal Surgery Division, Department of Cardiothoracic, Vascular Surgery and Organ Transplantation, Policlinico Umberto I University Hospital, Sapienza University of Rome, Viale del Policlinico 155, Rom, Italien
| | - Manuel Barberio
- Institute of Image-Guided Surgery, IHU-Strasbourg, Straßburg, Frankreich
- Research Institute against Cancer of the Digestive System, IRCAD, Straßburg, Frankreich
| | - Giancarlo D'Ambrosio
- General and Colorectal Surgery Division, Department of Cardiothoracic, Vascular Surgery and Organ Transplantation, Policlinico Umberto I University Hospital, Sapienza University of Rome, Viale del Policlinico 155, Rom, Italien
| | - Jacques Marescaux
- Institute of Image-Guided Surgery, IHU-Strasbourg, Straßburg, Frankreich
- Research Institute against Cancer of the Digestive System, IRCAD, Straßburg, Frankreich
| | - Michele Diana
- Institute of Image-Guided Surgery, IHU-Strasbourg, Straßburg, Frankreich
- Research Institute against Cancer of the Digestive System, IRCAD, Straßburg, Frankreich
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Faron M, Laas E. [Does sentinel lymph node identification has indication in digestive cancers?]. Bull Cancer 2019; 107:660-665. [PMID: 31627907 DOI: 10.1016/j.bulcan.2019.06.013] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2019] [Accepted: 06/03/2019] [Indexed: 11/30/2022]
Abstract
Despite being a standard of care in several cancers, sentinel lymph node (SLN) is not widespread in digestive cancers. European guidelines do not recommend its use for any digestive cancers. Particularity of the lymphatic vessel, intimately linked to blood vessel, may explain part of this phenomenon. Nevertheless, more indication could arise in the near future with the early diagnosis of tumor induced by cancer screening. Ruling out the lymphatic invasion could allow preserving the organ currently resected because of risk of lymph node positivity. This procedure is well studied in early gastric cancer in Korea and Japan. Several study have demonstrated that, a dual-tracer (isotopic and dye) allows to accurately identify the SLN. A randomized phase 3 trial is currently active in Korea to evaluate the oncological results of the procedure. Similar indication could arise for T1 tumor of the low-rectum, but currently available data are insufficient to recommend its use outside of a study. SLN may also be used to detect aberrant lymphatic drainage (rectum, ileum) but have been tested so far only in a few dozen of patients. Finally, SLN is disappointing in colon cancer, due to its low sensitivity and the absence of modification of the surgical procedure induced.
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Affiliation(s)
- Matthieu Faron
- Gustave-Roussy Cancer Campus, département de chirurgie viscérale oncologique, 114, rue Édouard-Vaillant, 94805 Villejuif cedex, France; Unité Inserm 1018 CESP Oncostat, Gustave-Roussy Cancer Campus, département de biostatistiques et épidémiologie, 114, rue Édouard-Vaillant, 94805 Villejuif cedex, France.
| | - Enora Laas
- Institut Curie, service de chirurgie senologique, gynécologique et reconstructrice, 26, rue d'Ulm, 75005 Paris, France
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Qi C, Zhang H, Chen Y, Su S, Wang X, Huang X, Fang C, Li B, Xia X, He P. Effectiveness and safety of indocyanine green fluorescence imaging-guided hepatectomy for liver tumors: A systematic review and first meta-analysis. Photodiagnosis Photodyn Ther 2019; 28:346-353. [PMID: 31600578 DOI: 10.1016/j.pdpdt.2019.10.007] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/06/2019] [Revised: 09/29/2019] [Accepted: 10/04/2019] [Indexed: 12/13/2022]
Abstract
BACKGROUND This meta-analysis was conducted to evaluate the effectiveness and safety of indocyanine green fluorescence imaging-guided hepatectomy(FIGH) for liver tumors. METHODS Clinical studies were retrieved from the PubMed, Embase, Cochrane Library, Medline and Web of Science electronic databases. Primary outcomes included operative time, blood loss, blood transfusion, hospital stay, R0 resection, postoperative complications, postoperative mortality and 1-year recurrence rate. Study-specific effect sizes and their 95% confidence intervals (CIs) were combined to calculate the pooled value using a fixed-effects or random-effects model. RESULTS Six studies comprising 587 patients were included. Major operative time (mean difference [MD] = -55.45; 95% CI = -78.85- -32.05), blood loss (MD = 12.99; 95% CI = 12.00-13.97), hospital stay (rate difference [RD] = -12.61; 95% CI = -15.06- -10.17), and postoperative complications (RD = -0.07; 95% CI = -0.12- -0.01) were all less in the FIGH group than in the traditional hepatectomy(TH) group. No differences were found in blood transfusion, R0 resection or 1-year recurrence rate. No perioperative mortality was observed in either group. CONCLUSION Based on current evidence, applying indocyanine green fluorescence imaging technology to accurately diagnose and treat liver tumors can effectively reduce operative time, blood loss, hospital stay and postoperative complications.
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Affiliation(s)
- Chi Qi
- Department of Nuclear Medicine, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China; Nuclear Medicine and Molecular Imaging Key Laboratory of Sichuan Province, Luzhou, 646000, China
| | - Hao Zhang
- Department of Hepatobiliary Surgery, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China
| | - Yue Chen
- Department of Nuclear Medicine, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China; Nuclear Medicine and Molecular Imaging Key Laboratory of Sichuan Province, Luzhou, 646000, China
| | - Song Su
- Department of Hepatobiliary Surgery, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China
| | - XiaoFeng Wang
- Department of Radiology, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China
| | - XinQiao Huang
- Department of Radiology, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China
| | - Cheng Fang
- Department of Hepatobiliary Surgery, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China
| | - Bo Li
- Department of Hepatobiliary Surgery, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China
| | - XianMing Xia
- Department of Hepatobiliary Surgery, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China; Academician(Expert)Workstation of Sichuan Province, Luzhou, 646000, China.
| | - Pan He
- Department of Hepatobiliary Surgery, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China; Academician(Expert)Workstation of Sichuan Province, Luzhou, 646000, China; Department of Anesthesiology, Affiliated Hospital, Southwest Medical University, Luzhou, 646000, China.
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Esposito F, Noviello A, Moles N, Coppola Bottazzi E, Baiamonte M, Macaione I, Ferbo U, Lepore M, Miro A, Crafa F. Sentinel Lymph Node Analysis in Colorectal Cancer Patients Using One-Step Nucleic Acid Amplification in Combination With Fluorescence and Indocyanine Green. Ann Coloproctol 2019; 35:174-180. [PMID: 31487764 PMCID: PMC6732328 DOI: 10.3393/ac.2018.07.21.1] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/13/2018] [Accepted: 07/21/2018] [Indexed: 02/06/2023] Open
Abstract
PURPOSE Analysis of the sentinel lymph node (SLN) in colorectal cancer (CRC) patients was proposed for more accurate staging and tailored lymphadenectomy. The aim of this study was to assess the ability to predict lymph node (LN) involvement through analysis of the SLN with a one-step nucleic acid (OSNA) technique in combination with peritumoral injection of indocyanine green (ICG) and near-infrared (NIR) lymphangiography in CRC patients. METHODS A total of 34 patients were enrolled. Overall, 51 LNs were analyzed with OSNA. LNs of 17 patients (50%) were examined simultaneously with hematoxylin and eosin (H&E) and OSNA. RESULTS SLN analysis of 17 patients examined with H&E and OSNA revealed that OSNA had a higher sensitivity (1 vs. 0.55), higher negative predictive value (1 vs. 0.66) and higher accuracy (100% vs. 76.4%) in predicting LN involvement. Overall, OSNA showed a sensitivity of 0.69, specificity of 1, accuracy of 88.2%, and stage migration of 8.8%. Compared to those who were OSNA (-), OSNA (+) patients had a greater number of LN metastases (4.8 vs. 0.16, P = 0.04), higher G3 rate (44.4% vs. 4%, P = 0.01), more advanced stage of disease (stage III: 77.8% vs. 16%; P = 0.00) and were more rapidly subjected to adjuvant chemotherapy (39.1 days vs. 50.2 days, P = 0.01). CONCLUSION SLN analysis with OSNA in combination with ICG-NIR lymphangiography is feasible and can detect LN involvement in CRC patients. Furthermore, it allows for more accurate staging reducing the delay between surgery and adjuvant chemotherapy.
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Affiliation(s)
- Francesco Esposito
- Oncological and General Surgery Unit, St. Giuseppe Moscati Hospital of National Relevance and High Specialty, Avellino, Italy
| | - Adele Noviello
- Oncological and General Surgery Unit, St. Giuseppe Moscati Hospital of National Relevance and High Specialty, Avellino, Italy
| | - Nicola Moles
- Oncological and General Surgery Unit, St. Giuseppe Moscati Hospital of National Relevance and High Specialty, Avellino, Italy
| | - Enrico Coppola Bottazzi
- Oncological and General Surgery Unit, St. Giuseppe Moscati Hospital of National Relevance and High Specialty, Avellino, Italy
| | - Mario Baiamonte
- General and Emergency Surgery Unit, Civico Benfratelli Di Cristina Hospital, Palermo, Italy
| | - Ina Macaione
- Department of Surgical, Oncological and Stomatological Disciplines, University of Palermo, Palermo, Italy
| | - Umberto Ferbo
- Institute of Pathology, St. Giuseppe Moscati Hospital of National Relevance and High Specialty, Avellino, Italy
| | - Maria Lepore
- Institute of Pathology, St. Giuseppe Moscati Hospital of National Relevance and High Specialty, Avellino, Italy
| | - Antonio Miro
- Oncological and General Surgery Unit, St. Giuseppe Moscati Hospital of National Relevance and High Specialty, Avellino, Italy
| | - Francesco Crafa
- Oncological and General Surgery Unit, St. Giuseppe Moscati Hospital of National Relevance and High Specialty, Avellino, Italy
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Zhou SC, Tian YT, Wang XW, Zhao CD, Ma S, Jiang J, Li EN, Zhou HT, Liu Q, Liang JW, Zhou ZX, Wang XS. Application of indocyanine green-enhanced near-infrared fluorescence-guided imaging in laparoscopic lateral pelvic lymph node dissection for middle-low rectal cancer. World J Gastroenterol 2019; 25:4502-4511. [PMID: 31496628 PMCID: PMC6710176 DOI: 10.3748/wjg.v25.i31.4502] [Citation(s) in RCA: 47] [Impact Index Per Article: 7.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/26/2019] [Revised: 07/08/2019] [Accepted: 07/19/2019] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND As one effective treatment for lateral pelvic lymph node (LPLN) metastasis (LPNM), laparoscopic LPLN dissection (LPND) is limited due to the complicated anatomy of the pelvic sidewall and various complications after surgery. With regard to improving the accuracy and completeness of LPND as well as safety, we tried an innovative method using indocyanine green (ICG) visualized with a near-infrared (NIR) camera system to guide the detection of LPLNs in patients with middle-low rectal cancer. AIM To investigate whether ICG-enhanced NIR fluorescence-guided imaging is a better technique for LPND in patients with rectal cancer. METHODS A total of 42 middle-low rectal cancer patients with clinical LPNM who underwent total mesorectal excision (TME) and LPND between October 2017 and March 2019 at our institution were assessed and divided into an ICG group and a non-ICG group. Clinical characteristics, operative outcomes, pathological outcomes, and postoperative complication information were compared and analysed between the two groups. RESULTS Compared to the non-ICG group, the ICG group had significantly lower intraoperative blood loss (55.8 ± 37.5 mL vs 108.0 ± 52.7 mL, P = 0.003) and a significantly larger number of LPLNs harvested (11.5 ± 5.9 vs 7.1 ± 4.8, P = 0.017). The LPLNs of two patients in the non-IVG group were residual during LPND. In addition, no significant difference was found in terms of LPND, LPNM, operative time, conversion to laparotomy, preoperative complication, or hospital stay (P > 0.05). CONCLUSION ICG-enhanced NIR fluorescence-guided imaging could be a feasible and convenient technique to guide LPND because it could bring specific advantages regarding the accuracy and completeness of surgery as well as safety.
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Affiliation(s)
- Si-Cheng Zhou
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Yan-Tao Tian
- Department of Pancreatic and Gastric Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Xue-Wei Wang
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Chuan-Duo Zhao
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Shuai Ma
- Department of Pancreatic and Gastric Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Jun Jiang
- Department of Radiology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Er-Ni Li
- Department of Radiology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Hai-Tao Zhou
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Qian Liu
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Jian-Wei Liang
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Zhi-Xiang Zhou
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
| | - Xi-Shan Wang
- Department of Colorectal Surgery, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
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He P, Su S, Fang C, He K, Chi C, Xia X, Tian J, Li B. Residual cancerous lesion and vein tumour thrombus identified intraoperatively using a fluorescence navigation system in liver surgery. ANZ J Surg 2019; 89:E308-E314. [PMID: 31218810 DOI: 10.1111/ans.15282] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/20/2019] [Revised: 03/26/2019] [Accepted: 04/16/2019] [Indexed: 01/06/2023]
Abstract
AIM The main aims of this study are to investigate the clinical application value of using indocyanine green fluorescence imaging for ensuring complete resection of tumour tissue during hepatectomy and to evaluate the diagnostic efficacy of near-infrared (NIR) fluorescence imaging system using indocyanine green in hepatectomy. METHODS After undergoing liver resection at the Affiliated Hospital of Southwest Medical University from July 2017 to May 2018, 35 eligible patients were included in this study. The liver surface and resection margin were intraoperatively assessed by intraoperative ultrasonography and NIR fluorescence imaging, after intravenous administration of indocyanine green (0.5 mg/kg) 72-96 h prior to surgery. The intraoperative observations were compared with the pathological findings in the liver. RESULTS In the 35 patients, a total of 53 lesions were found, of which 42 were malignant lesions. The analysis results showed that the sensitivity and accuracy of detection using NIR fluorescence imaging were significantly higher than with intraoperative ultrasonography (P < 0.05). However, there was no difference between contrast-enhanced helical computed tomography and NIR fluorescence imaging in finding lesions (P > 0.05). In addition, 11 new suspicious lesions were detected only by NIR fluorescence imaging in the liver surface and resection margin during surgery, four of which were hepatocellular carcinoma. We also detected four vein tumour thrombi using the NIR fluorescence navigation system. CONCLUSIONS The NIR fluorescence navigation system enables the identification of small tumours, residual cancer tissues in resection margin and venous tumour embolies in real time and enhances the accuracy and integrity of liver resection.
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Affiliation(s)
- Pan He
- Department of Hepatobiliary Surgery, Affiliated Hospital of Southwest Medical University, Luzhou, China.,Department of Anesthesiology, Affiliated Hospital of Southwest Medical University, Luzhou, China
| | - Song Su
- Department of Hepatobiliary Surgery, Affiliated Hospital of Southwest Medical University, Luzhou, China
| | - Cheng Fang
- Department of Hepatobiliary Surgery, Affiliated Hospital of Southwest Medical University, Luzhou, China
| | - Kai He
- Department of Hepatobiliary Surgery, Affiliated Hospital of Southwest Medical University, Luzhou, China
| | - Chongwei Chi
- Key Laboratory of Molecular Imaging, Institute of Automation, Chinese Academy of Sciences, Beijing, China.,Beijing Digital Precision Medicine Technology Co. Ltd., Beijing, China
| | - Xianming Xia
- Department of Hepatobiliary Surgery, Affiliated Hospital of Southwest Medical University, Luzhou, China
| | - Jie Tian
- Key Laboratory of Molecular Imaging, Institute of Automation, Chinese Academy of Sciences, Beijing, China
| | - Bo Li
- Department of Hepatobiliary Surgery, Affiliated Hospital of Southwest Medical University, Luzhou, China
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Kim HJ, Choi GS, Park JS, Park SY, Cho SH, Seo AN, Yoon GS. S122: impact of fluorescence and 3D images to completeness of lateral pelvic node dissection. Surg Endosc 2019; 34:469-476. [PMID: 31139999 DOI: 10.1007/s00464-019-06830-x] [Citation(s) in RCA: 24] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/27/2018] [Accepted: 05/14/2019] [Indexed: 12/12/2022]
Abstract
BACKGROUND Lateral pelvic lymph node dissection (LPND) is a technically demanding procedure. Consequently, there is a possibility of incomplete dissection of lateral pelvic lymph nodes (LPNs). We aimed to identify metastatic LPNs intraoperatively in real-time under dual guidance of fluorescence imaging and 3D lymphovascular reconstruction, and then to remove them completely. METHODS Rectal cancer patients who were scheduled to undergo LPND after preoperative chemoradiotherapy (CRT) were prospectively enrolled. We traced changes in suspected metastatic LPNs during preoperative CRT and defined them as index LPNs on post-CRT imaging studies. For fluorescence imaging, indocyanine green (ICG) at a dose of 2.5 mg was injected transanally around the tumor before the operation. For 3D reconstruction images, each patient underwent preoperative axial CT scan with contrast (0.6 mm slice thickness). These images were then manipulated with OsiriX. Index LPNs and essential structures in the pelvic sidewall, such as the obturator nerve, were reconstructed with abdominal arteries from 3D volume rendering. All surgical procedures were performed via laparoscopic or robotic approach. RESULTS From March to July 2017, ten rectal cancer patients underwent total mesorectal excision with LPND after preoperative CRT under dual image guidance. Bilateral LPND was performed in five patients. All index LPNs among ICG-bearing lymph nodes were clearly identified intraoperatively by matching with their corresponding 3D images. Pathologic LPN metastasis was confirmed in four patients (40.0%) and in five of the 15 dissected pelvic sidewalls (33.0%). All metastatic LPNs were identified among index LPNs. Four (80.0%) of the five metastatic LPNs were located in the internal iliac area. CONCLUSION Index LPNs among ICG-bearing lymph nodes in pelvic sidewall were clearly identified and completely removed by matching with their corresponding 3D reconstruction images. Further studies and long-term oncologic outcomes are required to determine the real impact of dual image guidance in LPND.
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Affiliation(s)
- Hye Jin Kim
- Colorectal Cancer Center, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, 807 Hogukro, Buk-gu, Daegu, 41404, South Korea
| | - Gyu-Seog Choi
- Colorectal Cancer Center, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, 807 Hogukro, Buk-gu, Daegu, 41404, South Korea.
| | - Jun Seok Park
- Colorectal Cancer Center, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, 807 Hogukro, Buk-gu, Daegu, 41404, South Korea
| | - Soo Yeun Park
- Colorectal Cancer Center, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, 807 Hogukro, Buk-gu, Daegu, 41404, South Korea
| | - Seung Hyun Cho
- Department of Radiology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, Daegu, South Korea
| | - An Na Seo
- Department of Pathology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, Daegu, South Korea
| | - Ghuil Suk Yoon
- Department of Pathology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, Daegu, South Korea
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Amano K, Aihara Y, Tsuzuki S, Okada Y, Kawamata T. Application of indocyanine green fluorescence endoscopic system in transsphenoidal surgery for pituitary tumors. Acta Neurochir (Wien) 2019; 161:695-706. [PMID: 30762125 DOI: 10.1007/s00701-018-03778-0] [Citation(s) in RCA: 24] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2018] [Accepted: 12/18/2018] [Indexed: 12/23/2022]
Abstract
BACKGROUND For the precise removal of pituitary tumors, preserving the surrounding normal structures, we need real-time intraoperative information on tumor location, margins, and surrounding structures. The aim of this study was to evaluate the benefits of a new intraoperative real-time imaging modality using indocyanine green (ICG) fluorescence through an endoscopic system during transsphenoidal surgery (TSS) for pituitary tumors. METHODS Between August 2013 and October 2014, 20 patients with pituitary and parasellar region tumors underwent TSS using the ICG fluorescence endoscopic system. We used a peripheral vein bolus dose of 6.25 mg/injection of ICG, started with a time counter, and examined how each tissue type increased and decreased in fluorescence through time. RESULTS A total of 33 investigations were performed for 20 patients: 9 had growth hormone secreting adenomas, 6 non-functioning pituitary adenomas, 3 Rathke's cleft cysts, 1 meningioma, and 1 pituicytoma. After the injection of ICG, the intensity of fluorescence of tumor and normal tissues under near-infrared light showed clear differences. We could differentiate tumor margins from adjacent normal tissues and define clearly the surrounding normal structures using the different fluorescent intensities time changes and tissue-specific fluorescence patterns. CONCLUSIONS The ICG endoscopic system is simple, user-friendly, quick, cost-effective, and reliable. The method offered real-time information during TSS to delimit pituitary and parasellar region tumor tissue from surrounding normal structures. This method can contribute to the improvement of total removal rates of tumors, reduction of complications after TSS, saving surgical time, and preserving endocrinological functions.
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Affiliation(s)
- Kosaku Amano
- Department of Neurosurgery, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo, 162-8666, Japan.
| | - Yasuo Aihara
- Department of Neurosurgery, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo, 162-8666, Japan
| | - Shunsuke Tsuzuki
- Department of Neurosurgery, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo, 162-8666, Japan
| | - Yoshikazu Okada
- Department of Neurosurgery, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo, 162-8666, Japan
| | - Takakazu Kawamata
- Department of Neurosurgery, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo, 162-8666, Japan
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Hsu CW. Lymph node mapping and anastomosis evaluation by VISERA ELITE II ® , a novel surgical endoscope system, with infrared fluorescence imaging during laparoscopic rectal cancer surgery - a video vignette. Colorectal Dis 2019; 21:375-376. [PMID: 30632256 DOI: 10.1111/codi.14555] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/24/2018] [Accepted: 12/21/2018] [Indexed: 12/13/2022]
Affiliation(s)
- C-W Hsu
- Department of Surgery, Kaohsiung Veteran General Hospital, Kaohsiung City, Taiwan.,Faculty of Medicine, National Yang-Ming University, Taipei, Taiwan
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Currie A. Intraoperative Sentinel Node Mapping in the Colon: Potential and Pitfalls. Eur Surg Res 2019; 60:45-52. [DOI: 10.1159/000494833] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/25/2018] [Accepted: 10/25/2018] [Indexed: 11/19/2022]
Abstract
Sentinel lymph node mapping (SLNM) may play a significant role in future delivery of colon cancer surgery because of an increase in early-stage, node-negative disease due to national bowel cancer screening programmes. Traditionally, colon lymphatic drainage has not been thought relevant as the operative approach cannot be tailored. Recent advances in local and endoscopic risk-reducing interventions for colonic malignancy have caused a rethink in approach. SLNM was initially attempted with blue dye techniques with limited success. Technological improvement has allowed surgeons to use near-infrared (NIR) light and NIR active tracers such as indocyanine green. This review provides an overview of the current status of intraoperative lymph node mapping in the colon, identifies challenges to the delivery of the techniques, and discusses potential solutions that may help SLNM play a role in improving the delivery of surgical care for patients with colon cancer.
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Singh R, Dumlupinar G, Andersson-Engels S, Melgar S. Emerging applications of upconverting nanoparticles in intestinal infection and colorectal cancer. Int J Nanomedicine 2019; 14:1027-1038. [PMID: 30799920 PMCID: PMC6369841 DOI: 10.2147/ijn.s188887] [Citation(s) in RCA: 35] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/21/2022] Open
Abstract
Colorectal cancer is the abnormal growth of cells in colon or rectum. Recent findings have acknowledged the role of bacterial infection and chronic inflammation in colorectal cancer initiation and progression. In order to detect and treat precancerous lesions, new tools are required, which may help to prevent or identify colorectal cancer at an early stage. To date, several different screening tests are available, including endoscopy, stool-based blood tests, and radiology-based tests. However, these analyses either lack sensitivity or are of an invasive nature. The use of fluorescently labeled probes can increase the detection sensitivity. However, autofluorescence, photobleaching, and photodamage are commonly encountered problems with fluorescence imaging. Upconverting nanoparticles (UCNPs) are recently developed lanthanide-doped nanocrystals that can be used as light-triggered luminescent probes and in drug delivery systems. In this review, we comprehensively summarize the recent developments and address future prospects of UCNP-based applications for diagnostics and therapeutic approaches associated with intestinal infection and colorectal cancer.
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Affiliation(s)
- Raminder Singh
- APC Microbiome Ireland, University College Cork, Cork, Ireland,
- School of Medicine, University College Cork, Cork, Ireland
| | - Gokhan Dumlupinar
- Irish Photonics Integration Centre, Tyndall National Institute, Cork, Ireland
- Department of Physics, University College Cork, Cork, Ireland
| | - Stefan Andersson-Engels
- Irish Photonics Integration Centre, Tyndall National Institute, Cork, Ireland
- Department of Physics, University College Cork, Cork, Ireland
| | - Silvia Melgar
- APC Microbiome Ireland, University College Cork, Cork, Ireland,
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Rapid detection of metastatic lymph nodes of colorectal cancer with a gamma-glutamyl transpeptidase-activatable fluorescence probe. Sci Rep 2018; 8:17781. [PMID: 30542087 PMCID: PMC6290796 DOI: 10.1038/s41598-018-36062-3] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/08/2018] [Accepted: 11/09/2018] [Indexed: 12/18/2022] Open
Abstract
Rapid diagnosis of metastatic lymph nodes (mLNs) of colorectal cancer (CRC) is desirable either intraoperatively or in resected fresh specimens. We have developed a series of activatable fluorescence probes for peptidase activities that are specifically upregulated in various tumors. We aimed to discover a target enzyme for detecting mLNs of CRC. Among our probes, we found that gGlu-HMRG, a gamma-glutamyl transpeptidase (GGT)-activatable fluorescence probe, could detect mLNs. This was unexpected, because we have previously reported that gGlu-HMRG could not detect primary CRC. We confirmed that the GGT activity of mLNs was high, whereas that of non-metastatic lymph nodes and CRC cell lines was low. We investigated the reason why GGT activity was upregulated in mLNs, and found that GGT was induced under conditions of hypoxia or low nutritional status. We utilized this feature to achieve rapid detection of mLNs with gGlu-HMRG. GGT appears to be a promising candidate enzyme for fluorescence imaging of mLNs.
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Liberale G, Bohlok A, Bormans A, Bouazza F, Galdon MG, El Nakadi I, Bourgeois P, Donckier V. Indocyanine green fluorescence imaging for sentinel lymph node detection in colorectal cancer: A systematic review. Eur J Surg Oncol 2018; 44:1301-1306. [DOI: 10.1016/j.ejso.2018.05.034] [Citation(s) in RCA: 18] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/30/2018] [Revised: 03/26/2018] [Accepted: 05/30/2018] [Indexed: 01/09/2023] Open
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van Manen L, Handgraaf HJM, Diana M, Dijkstra J, Ishizawa T, Vahrmeijer AL, Mieog JSD. A practical guide for the use of indocyanine green and methylene blue in fluorescence-guided abdominal surgery. J Surg Oncol 2018; 118:283-300. [PMID: 29938401 PMCID: PMC6175214 DOI: 10.1002/jso.25105] [Citation(s) in RCA: 200] [Impact Index Per Article: 28.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/23/2018] [Accepted: 04/21/2018] [Indexed: 12/14/2022]
Abstract
Near-infrared (NIR) fluorescence imaging is gaining clinical acceptance over the last years and has been used for detection of lymph nodes, several tumor types, vital structures and tissue perfusion. This review focuses on NIR fluorescence imaging with indocyanine green and methylene blue for different clinical applications in abdominal surgery with an emphasis on oncology, based on a systematic literature search. Furthermore, practical information on doses, injection times, and intraoperative use are provided.
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Affiliation(s)
- Labrinus van Manen
- Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands
| | | | - Michele Diana
- IHU-Strasbourg, Institute of Image-Guided Surgery, Strasbourg, France.,IRCAD, Research Institute against Cancer of the Digestive System, Strasbourg, France.,Department of General, Digestive and Endocrine Surgery, University Hospital of Strasbourg, Strasbourg, France
| | - Jouke Dijkstra
- Division of Image Processing, Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands
| | - Takeaki Ishizawa
- Hepato-Biliary-Pancreatic Surgery Division, Department of Surgery, Graduate School of Medicine, University of Tokyo, Tokyo, Japan
| | | | - Jan Sven David Mieog
- Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands
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Nanashima A, Tominaga T, Sumida Y, Tobinaga S, Nagayasu T. Indocyanine green identification for tumor infiltration or metastasis originating from hepatocellular carcinoma. Int J Surg Case Rep 2018; 46:56-61. [PMID: 29684806 PMCID: PMC6000743 DOI: 10.1016/j.ijscr.2018.03.044] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/10/2018] [Revised: 03/14/2018] [Accepted: 03/31/2018] [Indexed: 01/31/2023] Open
Abstract
The indocyanine green-photodynamic eye (ICG-PDE) system was useful to clearly detect metastasis or tumor thrombus, as well as main tumor, originated from hepatocellular carcinoma and all lesions could be resected. This system may be applied to improve determining the location of metastasis or tumor thrombus. Tumor thrombus originated from hepatocellular carcinoma (HCC) in the portal vein or inferior vena cava could be well identified by ICG-PDE. The metastasized HCC lesion in an adrenal gland was clearly detected. All lesions could be completely resected. ICG-PDE is a useful tool for detecting the precise tumor location even in extrahepatic tumor lesions or tumor thrombus, which is useful for deciding which parts to resect. Introduction The indocyanine green-photodynamic eye (ICG-PDE) system is useful to detect small hypervascular liver tumors, hepatocellular carcinoma (HCC), on the liver surface. This system may be also applied to improve determining the location of metastasis or tumor thrombus (TT). We herein report three case reports. ICG was administered preoperatively for functional testing and images of the tumor were observed during hepatectomy using a PDE camera. Case series The patient in case 1 exhibited advanced HCC with TT in the portal trunk. The TT in the right portal vein was clearly fluorescent by ICG-PDE and the right portal vein was adequately transected to remove TT. The patient in case 2 exhibited a large HCC in the right liver and the right adrenal gland was simultaneously swollen with enhancement. By confirming the fluorescent spot in the right adrenal gland, the metastasized lesion was completely resected. The patient in case 3 previously underwent central bi-segmentectomy, and lymph node metastasis and TT in the vena cava was observed during one-year follow-up. Although it was difficult to detect the definite margin of these lesions by the outline appearance, both lesions could be clearly observed with strong fluorescence and were completely resected. Discussion and conclusion ICG-PDE is a useful tool for detecting the precise tumor location even in extrahepatic tumor lesions, such as metastases or tumor thrombus, which is useful for deciding which parts to resect.
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Affiliation(s)
- Atsushi Nanashima
- Division of Hepato-biliary-pancreas and Digestive Surgery, Department of Surgery, University of Miyazaki Faculty of Medicine, Kiyotake 5200, Miyazaki, 889-1692, Japan; Department of Surgical Oncology, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan.
| | - Tetsuro Tominaga
- Department of Surgical Oncology, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan
| | - Yorihisa Sumida
- Department of Surgical Oncology, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan
| | - Shuichi Tobinaga
- Department of Surgical Oncology, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan
| | - Takeshi Nagayasu
- Department of Surgical Oncology, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan
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Ito A, Ohta M, Kato Y, Inada S, Kato T, Nakata S, Yatabe Y, Goto M, Kaneda N, Kurita K, Nakanishi H, Yoshida K. A Real-Time Near-Infrared Fluorescence Imaging Method for the Detection of Oral Cancers in Mice Using an Indocyanine Green-Labeled Podoplanin Antibody. Technol Cancer Res Treat 2018; 17:1533033818767936. [PMID: 29649929 PMCID: PMC5900824 DOI: 10.1177/1533033818767936] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/02/2023] Open
Abstract
Podoplanin is distinctively overexpressed in oral squamous cell carcinoma than oral benign neoplasms and plays a crucial role in the pathogenesis and metastasis of oral squamous cell carcinoma but its diagnostic application is quite limited. Here, we report a new near-infrared fluorescence imaging method using an indocyanine green (ICG)-labeled anti-podoplanin antibody and a desktop/a handheld ICG detection device for the visualization of oral squamous cell carcinoma-xenografted tumors in nude mice. Both near-infrared imaging methods using a desktop (in vivo imaging system: IVIS) and a handheld device (photodynamic eye: PDE) successfully detected oral squamous cell carcinoma tumors in nude mice in a podoplanin expression-dependent manner with comparable sensitivity. Of these 2 devices, only near-infrared imaging methods using a handheld device visualized oral squamous cell carcinoma xenografts in mice in real time. Furthermore, near-infrared imaging methods using the handheld device (PDE) could detect smaller podoplanin-positive oral squamous cell carcinoma tumors than a non-near-infrared, autofluorescence-based imaging method. Based on these results, a near-infrared imaging method using an ICG-labeled anti-podoplanin antibody and a handheld detection device (PDE) allows the sensitive, semiquantitative, and real-time imaging of oral squamous cell carcinoma tumors and therefore represents a useful tool for the detection and subsequent monitoring of malignant oral neoplasms in both preclinical and some clinical settings.
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Affiliation(s)
- Akihiro Ito
- 1 Graduate School of Pharmaceutical Sciences, Meijo University, Nagoya, Japan.,2 Department of Pathology and Molecular Diagnostics, Aichi Cancer Center Central Hospital, Nagoya, Japan
| | - Mitsuhiko Ohta
- 3 The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan.,4 Department of Oral and Maxillofacial Surgery, Daiyukai General Hospital, Ichinomiya, Japan
| | - Yukinari Kato
- 5 Department of Regional Innovation, Tohoku University Graduate School of Medicine, Sendai, Japan
| | - Shunko Inada
- 6 Information and Communications Headquarters/Graduate School of Information Science, Nagoya University, Nagoya, Japan
| | - Toshio Kato
- 7 Department of Diagnostic Pathology, Daiyukai General Hospital, Ichinomiya, Japan
| | - Susumu Nakata
- 8 Department of Clinical Oncology, Kyoto Pharmaceutical University, Kyoto, Japan
| | - Yasushi Yatabe
- 2 Department of Pathology and Molecular Diagnostics, Aichi Cancer Center Central Hospital, Nagoya, Japan
| | - Mitsuo Goto
- 3 The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan
| | - Norio Kaneda
- 1 Graduate School of Pharmaceutical Sciences, Meijo University, Nagoya, Japan
| | - Kenichi Kurita
- 3 The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan
| | - Hayao Nakanishi
- 2 Department of Pathology and Molecular Diagnostics, Aichi Cancer Center Central Hospital, Nagoya, Japan.,9 Laboratory of Pathology and Clinical Research, Aichi Cancer Center Aichi Hospital, Okazaki, Japan
| | - Kenji Yoshida
- 3 The First Department of Oral and Maxillofacial Surgery, School of Dentistry, Aichi-Gakuin University, Nagoya, Japan
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