Abstract
Recently, fluorescence imaging following the preoperative intravenous injection of indocyanine green has been used in clinical settings to identify hepatic malignancies during surgery. The aim of this study was to evaluate the ability of photoacoustic tomography using indocyanine green as a contrast agent to produce representative fluorescence images of hepatic tumors by visualizing the spatial distribution of indocyanine green on ultrasonographic images. Indocyanine green (0.5 mg/kg, intravenous) was preoperatively administered to 9 patients undergoing hepatectomy. Intraoperatively, photoacoustic tomography was performed on the surface of the resected hepatic specimens (n = 10) under excitation with an 800 nm pulse laser. In 4 hepatocellular carcinoma nodules, photoacoustic imaging identified indocyanine green accumulation in the cancerous tissue. In contrast, in one hepatocellular carcinoma nodule and five adenocarcinoma foci (one intrahepatic cholangiocarcinoma and 4 colorectal liver metastases), photoacoustic imaging delineated indocyanine green accumulation not in the cancerous tissue but rather in the peri-cancerous hepatic parenchyma. Although photoacoustic tomography enabled to visualize spatial distribution of ICG on ultrasonographic images, which was consistent with fluorescence images on cut surfaces of the resected specimens, photoacoustic signals of ICG-containing tissues decreased approximately by 40% even at 4 mm depth from liver surfaces. Photoacoustic tomography using indocyanine green also failed to identify any hepatocellular carcinoma nodules from the body surface of model mice with non-alcoholic steatohepatitis. In conclusion, photoacoustic tomography has a potential to enhance cancer detectability and differential diagnosis by ultrasonographic examinations and intraoperative fluorescence imaging through visualization of stasis of bile-excreting imaging agents in and/or around hepatic tumors. However, further technical advances are needed to improve the visibility of photoacoustic signals emitted from deeply-located lesions.
Highlights
In vivo fluorescence imaging using indocyanine green (ICG) has been clinically applied as an intraoperative navigation tool that enables the real-time identification of biological structures, such as the lymphatic system [1,2] and the biliary ducts [3,4,5,6,7], as well as the evaluation of visceral blood perfusion [8,9,10,11]
Since 2008, ICG fluorescence imaging has been used to identify hepatic tumors during open hepatectomy [12,13,14,15] and, more recently, laparoscopic hepatectomy [16]. This technique is based on the accumulation of ICG, which is intravenously administered for preoperative liver function testing, in hepatocellular carcinoma (HCC) tissue and in the non-cancerous hepatic parenchyma located around adenocarcinoma foci, such as colorectal liver metastases (CRLM) and intrahepatic cholangiocarcinoma (ICC) [12]
When fluorescence images of the cut surfaces of resected specimens are obtained, well- to moderately-differentiated HCC shows uniform fluorescence of ICG in the cancerous tissue, while poorly differentiated HCC and adenocarcinoma show rim-type fluorescence around the tumor [17]. Both types of cancer-associated ICG fluorescence can be detected by commercially-available fluorescence imaging systems as far as the tumors are located beneath the liver surface, there is a need for novel imaging technology that enables the detection of deeply-located hepatic tumors and the visualization of ICG accumulation in and/ or around these lesions on cross-sectional images
Summary
In vivo fluorescence imaging using indocyanine green (ICG) has been clinically applied as an intraoperative navigation tool that enables the real-time identification of biological structures, such as the lymphatic system [1,2] and the biliary ducts [3,4,5,6,7], as well as the evaluation of visceral blood perfusion [8,9,10,11]. Photoacoustic (PA) tomography has been actively developed as a novel optical imaging technology that enables the real-time visualization of deeply-located biologic structures on ultrasonographic images through the ‘‘photoacoustic effect’’ [18,19,20]. With this technique, nanosecond laser pulses are transmitted into tissue and absorbed by endogenous chromophores or exogenous molecular imaging agents in targeted structures. The rapid absorption increases focal temperature and produces a thermoelastic expansion that creates acoustic waves These photoacoustic signals can be detected using ultrasound (US) receivers and used to reconstruct images of the targeted biological structures according to the absorbed optical energy density. The aim of this study was to evaluate the ability of PA tomography using ICG as a contrast agent to produce representative fluorescence images of hepatic tumors, using both surgically-resected human hepatic samples and a mouse model of HCC (mice with non-alcoholic steatohepatitis [NASH])
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