TY - JOUR
AU - Tanaka, N
AB - Abstract Background Three-dimensional (3D) imaging has facilitated liver resection with excision of hepatic veins by estimating the liver volume of portal and hepatic venous territories. However, 3D imaging cannot be used for real-time navigation to determine the liver transection line. This study assessed the value of indocyanine green (ICG) fluorescence imaging with hepatic vein clamping for navigation during liver transection. Methods Consecutive patients who underwent liver resection with excision of major hepatic veins between 2012 and 2013 were evaluated using ICG fluorescence imaging after clamping veins and injecting ICG. Regional fluorescence intensity (FI) values of non-veno-occlusive regions (FINon), veno-occlusive regions (FIVO) and ischaemic regions (FIIS) were calculated using luminance analysing software. Results Of the 21 patients, ten, four and seven underwent limited resection, monosegmentectomy/sectionectomy and hemihepatectomy respectively, with excision of major hepatic veins. Median veno-occlusive liver volume was 80 (range 30–458) ml. Fluorescence imaging visualized veno-occlusive regions as territories with lower FI compared with non-veno-occlusive regions, and ischaemic regions as territories with no fluorescence after intravenous ICG injection. Median FIIS/FINon was lower than median FIVO/FINon (0·22 versus 0·59; P = 0·002). There were no deaths in hospital or within 30 days, and only one major complication. Conclusion ICG fluorescence imaging with hepatic vein clamping visualized non-veno-occlusive, veno-occlusive and ischaemic regions. This technique may guide liver transection by intraoperative navigation, enhancing the safety and accuracy of liver resection. Introduction Recent developments in three-dimensional (3D) preoperative imaging and volumetric analysis have enabled accurate estimation of the liver volume of portal segments and hepatic venous territories. This has also facilitated liver resection with excision of hepatic veins1,2. These procedures are required to secure a surgical margin in patients with liver tumours adjacent to or involving hepatic veins3–5. Virtual imaging can be used for preoperative simulation or planning of liver resections. However, it cannot be used as a real-time guide to determine the transection line of the liver or to estimate regional hepatic perfusion domains while visualizing portal segments and/or hepatic venous territories on the liver surface. The technique of dye injection into the portal vein can be used for intraoperative navigation to identify portal segments of interest6. However, intraoperative navigation focusing on visualization of territories drained by hepatic veins has not yet been established. Recently, the hepatic uptake function of veno-occlusive regions in the remnant liver was evaluated using fluorescence imaging following systemic intravenous injection of indocyanine green (ICG)7. The results indicated that fluorescence intensity (FI) correlated with ICG concentration in liver tissue, implying that ICG fluorescence reflects hepatic perfusion levels. Hepatic uptake of ICG in veno-occlusive regions was 30–40 per cent of that in non-veno-occlusive regions. This study suggested that ICG fluorescence imaging with hepatic vein clamping may enable evaluation of the extent of hepatic venous drainage territories. The aim of this study was to evaluate the value of ICG fluorescence imaging with hepatic vessel clamping for navigation of liver transection by assessing the FI of temporarily clamped hepatic venous and portal venous territories. Methods This study was conducted with the approval of the Institutional Ethics Review Board of Asahi General Hospital. Written informed consent was obtained from all patients. Patients The study group consisted of consecutive patients who underwent liver resection with excision of major hepatic veins for malignant liver tumours adherent to hepatic veins at Asahi General Hospital between July 2012 and October 2013. Preoperative estimation of regional liver volume Parenchymal volumes of portal segments and hepatic venous territories were calculated using preoperative 3D CT and region-growing method software (Organ Volume Analysis; Hitachi Medico, Chiba, Japan)2,8–9. Total liver volume (TLV), remnant liver volume (RLV), veno-occlusive liver volume and non-veno-occlusive liver volume were calculated. Standard liver volume10 was defined as 706·2 × body surface area (m2) + 2·4 ml. Indications for liver resection were based on preoperative liver function parameters, such as the presence/absence of uncontrolled ascites, serum bilirubin level and ICG retention rate at 15 min (ICG-R15)11,12. Intraoperative ICG fluorescence evaluation after hepatic vein clamping During liver resections, ICG (2·5 µg per ml TLV, calculated from preoperative 3D CT data) was injected into peripheral veins after hepatic veins to be resected had been taped and clamped (venous clamp–ICG technique). The left (right) hepatic artery/portal vein were also clamped or ligated before ICG injection for extended left (right) hepatectomy to identify ischaemic and veno-occlusive regions. Fluorescence images of the liver surface were recorded for 300 s after ICG injection, with a fluorescence imaging camera system (PDE; Hamamatsu Photonics, Hamamatsu, Japan) positioned 20 cm above the liver surface and with surgical lights turned off13. The output of the light-emitting diodes (760 nm) was set at 0·21 mW/cm2. Subsequently, regional FI values of non-veno-occlusive regions (FINon), veno-occlusive regions (FIVO) and ischaemic regions (FIIS) were calculated using luminance analysing software (U11437; Hamamatsu Photonics). The transection line was determined during surgery to ensure the surgical margin and to leave no ischaemic regions. Veno-occlusive regions were preserved after noting the increase in ICG fluorescence that confirms the hepatic perfusion7. Outcomes of patients were monitored and complications were graded according to the Clavien–Dindo classification14. Statistical analysis Continuous data are expressed as median (range) and were compared using the Wilcoxon rank sum test. P < 0·050 was considered to denote statistical significance. Statistical analysis was performed with JMP® software version 9.0.2 (SAS Institute, Cary, North Carolina, USA). Results A total of 21 patients were enrolled in the study. Age ranged from 38 to 84 (median 67) years. Median preoperative ICG-R15 was 10·9 (4·5–34·5) per cent. Surgical procedures with excision of major hepatic veins were either limited resection (10), monosegmentectomy/sectionectomy (4) or hemihepatectomy (7) (Table 1). Table 1 Patient characteristics . No. of patients* (n = 21) . Preoperative characteristics Age (years)† 67 (38–84) Sex ratio (M : F) 15 : 6 BMI (kg/m2)† 22·4 (18·5–28·2) ASA fitness grade† II (I–III) Preoperative chemotherapy 9 Child–Pugh score† 6 (4–9) ICG-R15 (%)† 10·9 (4·5–34·5) Chronic hepatitis 9 Liver cirrhosis 4 Indication Colorectal liver metastases 9 Hepatocellular carcinoma 9 Others 3 Surgical procedure Limited resection‡ 10 Monosegmentectomy/sectionectomy§ 4 Hemihepatectomy¶ 7 . No. of patients* (n = 21) . Preoperative characteristics Age (years)† 67 (38–84) Sex ratio (M : F) 15 : 6 BMI (kg/m2)† 22·4 (18·5–28·2) ASA fitness grade† II (I–III) Preoperative chemotherapy 9 Child–Pugh score† 6 (4–9) ICG-R15 (%)† 10·9 (4·5–34·5) Chronic hepatitis 9 Liver cirrhosis 4 Indication Colorectal liver metastases 9 Hepatocellular carcinoma 9 Others 3 Surgical procedure Limited resection‡ 10 Monosegmentectomy/sectionectomy§ 4 Hemihepatectomy¶ 7 * Unless indicated otherwise; † values are median (range). ‡ With excision of left hepatic vein (LHV) (1), middle hepatic vein (MHV) (3) right hepatic vein (RHV) (5), and LHV and MHV (1); § with excision of LHV (2), MHV (1) and RHV (1); ¶ with excision of MHV (7). ICG-R15, indocyanine green retention rate at 15 min. Open in new tab Table 1 Patient characteristics . No. of patients* (n = 21) . Preoperative characteristics Age (years)† 67 (38–84) Sex ratio (M : F) 15 : 6 BMI (kg/m2)† 22·4 (18·5–28·2) ASA fitness grade† II (I–III) Preoperative chemotherapy 9 Child–Pugh score† 6 (4–9) ICG-R15 (%)† 10·9 (4·5–34·5) Chronic hepatitis 9 Liver cirrhosis 4 Indication Colorectal liver metastases 9 Hepatocellular carcinoma 9 Others 3 Surgical procedure Limited resection‡ 10 Monosegmentectomy/sectionectomy§ 4 Hemihepatectomy¶ 7 . No. of patients* (n = 21) . Preoperative characteristics Age (years)† 67 (38–84) Sex ratio (M : F) 15 : 6 BMI (kg/m2)† 22·4 (18·5–28·2) ASA fitness grade† II (I–III) Preoperative chemotherapy 9 Child–Pugh score† 6 (4–9) ICG-R15 (%)† 10·9 (4·5–34·5) Chronic hepatitis 9 Liver cirrhosis 4 Indication Colorectal liver metastases 9 Hepatocellular carcinoma 9 Others 3 Surgical procedure Limited resection‡ 10 Monosegmentectomy/sectionectomy§ 4 Hemihepatectomy¶ 7 * Unless indicated otherwise; † values are median (range). ‡ With excision of left hepatic vein (LHV) (1), middle hepatic vein (MHV) (3) right hepatic vein (RHV) (5), and LHV and MHV (1); § with excision of LHV (2), MHV (1) and RHV (1); ¶ with excision of MHV (7). ICG-R15, indocyanine green retention rate at 15 min. Open in new tab Preoperative regional liver volume Preoperative regional liver volumes with and without venous occlusion are summarized in Table 2. Regional liver volumes were not significantly different between patients with hepatocellular carcinoma (HCC) and those with colorectal liver metastases (Table S1, supporting information). Table 2 Preoperative estimation of regional liver volumes in 21 patients . Median (range) . Total liver volume (ml) 1091 (699–1532) Remnant liver volume (ml) 864 (584–1316) % total liver volume 86·6 (52·6–97·1) % standard liver volume* 88·3 (42·1–97·9) Veno-occlusive liver volume (ml) 80 (30–458) % remnant liver volume 10·1 (3·6–53·0) Non-veno-occlusive liver volume (ml) 756 (368–1222) % total liver volume 79·3 (37·2–92·7) % standard liver volume* 76·3 (23·8–94·6) . Median (range) . Total liver volume (ml) 1091 (699–1532) Remnant liver volume (ml) 864 (584–1316) % total liver volume 86·6 (52·6–97·1) % standard liver volume* 88·3 (42·1–97·9) Veno-occlusive liver volume (ml) 80 (30–458) % remnant liver volume 10·1 (3·6–53·0) Non-veno-occlusive liver volume (ml) 756 (368–1222) % total liver volume 79·3 (37·2–92·7) % standard liver volume* 76·3 (23·8–94·6) * Urata et al.10. Open in new tab Table 2 Preoperative estimation of regional liver volumes in 21 patients . Median (range) . Total liver volume (ml) 1091 (699–1532) Remnant liver volume (ml) 864 (584–1316) % total liver volume 86·6 (52·6–97·1) % standard liver volume* 88·3 (42·1–97·9) Veno-occlusive liver volume (ml) 80 (30–458) % remnant liver volume 10·1 (3·6–53·0) Non-veno-occlusive liver volume (ml) 756 (368–1222) % total liver volume 79·3 (37·2–92·7) % standard liver volume* 76·3 (23·8–94·6) . Median (range) . Total liver volume (ml) 1091 (699–1532) Remnant liver volume (ml) 864 (584–1316) % total liver volume 86·6 (52·6–97·1) % standard liver volume* 88·3 (42·1–97·9) Veno-occlusive liver volume (ml) 80 (30–458) % remnant liver volume 10·1 (3·6–53·0) Non-veno-occlusive liver volume (ml) 756 (368–1222) % total liver volume 79·3 (37·2–92·7) % standard liver volume* 76·3 (23·8–94·6) * Urata et al.10. Open in new tab Fluorescence intensity evaluation after hepatic vein clamping Median plateau FINon and FIVO were 168 (84–239) and 115 (36–195) respectively. The median FIVO/FINon ratio was 0·59 (0·36–0·92). In all seven patients who underwent extended right or left hepatectomy, the FI of ischaemic regions (corresponding to the hemiliver to be resected) did not increase. The median FIIS/FINon ratio was 0·22 (0·07–0·36), which was lower than the FIVO/FINon ratio (P = 0·002) (Fig. 1). The median FIVO/FINon ratio was not significantly different between patients with and those without liver cirrhosis (0·54 (0·43–0·73) versus 0·63 (0·36–0·92); P = 0·347), and between patients who underwent preoperative chemotherapy and those who did not (0·65 (0·49–0·92) versus 0·59 (0·36–0·81); P = 0·241). Fig. 1 Open in new tabDownload slide Plateau fluorescence intensity (FI) ratios of veno-occlusive and ischaemic regions compared with non-veno-occlusive regions. FINon, FI of non-veno-occlusive regions; FIVO, FI of veno-occlusive regions; FIIS, FI of ischaemic regions Application of the venous clamp–ICG technique Using the venous clamp–ICG technique, fluorescence imaging visualized veno-occlusive regions as territories with lower FI compared with non-veno-occlusive regions, and ischaemic regions as territories with no fluorescence after intravenous ICG injection (Fig. 1). Application to extended left hepatectomy with middle hepatic vein excision Details of a patient (ICG-R15 8·0 per cent) who underwent extended left hepatectomy with middle hepatic vein (MHV) excision for an 8·0-cm diameter colorectal liver metastasis invading the MHV located in segments IV and VIII are shown in Figs 2 and 3, and Video S1 (supporting information). The RLV was calculated as 744 ml (63·1 per cent of TLV). After clamping the MHV root, left hepatic artery and left portal vein, 1·18 ml ICG (2·5 mg/ml) was administered intravenously. The FI values on the liver surface increased linearly and then reached a plateau, providing a clear demarcation between regions with and without venous occlusion (plateau FI values 103 and 142 respectively). The FI values did not increase in regions without portal inflow (FI value 33). The transection line was tailored to ensure the surgical margin and not to leave ischaemic regions. The veno-occlusive regions were not resected after noting the increase in ICG fluorescence, confirming hepatic perfusion. After resection, fluorescence imaging visualized the regions with and without venous occlusion in the remnant liver. Fig. 2 Open in new tabDownload slide Application of indocyanine green (ICG) fluorescence imaging to extended left hepatectomy with middle hepatic vein (MHV) excision. a Preoperative simulation based on preoperative three-dimensional CT (left and middle images) and gross appearance of the liver before transection (right image). The total (TLV) and remnant (RLV) liver volumes were estimated as 1180 and 744 ml respectively. Regional volumes in the remnant liver were estimated as follows (middle image): veno-occlusive regions after division of the MHV (75 ml, 10·1 per cent of RLV; yellow arrowhead), non-veno-occlusive regions (669 ml, 56·7 per cent of TLV; arrow) and ischaemic regions after division of the left hepatic artery and portal vein (436 ml, 36·9 per cent of TLV; white arrowhead). b Temporary clamping of MHV. c Fluorescence intensity (FI) values on the liver surface increased linearly and then reached a plateau, providing a clear demarcation between non-veno-occlusive and veno-occlusive regions (clamped MHV territories), whereas the FI values did not increase in ischaemic regions (ligated left portal vein territories). Fig. 3 Open in new tabDownload slide Application of indocyanine green (ICG) fluorescence imaging extended to left hepatectomy with middle hepatic vein (MHV) excision. a Fluorescence imaging before (left image) and 240 s after (right image) intravenous injection of ICG (1·18 ml, 2·95 mg) revealed demarcation between veno-occlusive regions (plateau FI value 103; yellow arrowhead), non-veno-occlusive regions (plateau FI value 142; arrow) and ischaemic regions (FI value 33; white arrowhead). These findings were comparable to those of the preoperative imaging studies. b The border between veno-occlusive (yellow arrowhead) and non-veno-occlusive (arrow) regions was indistinguishable from the gross appearance of the liver surface, whereas ischaemic regions (white arrowhead) were clearly visualized (left image). The transection line was planned by referring to ICG fluorescence images while securing the surgical margin and leaving veno-occlusive regions. ICG fluorescence imaging identified the veno-occlusive regions in the remnant liver; gross appearance after extended left hepatectomy (middle image) and corresponding fluorescence image (right) are shown. See also Video S1 (supporting information) ICG fluorescence evaluation of middle hepatic vein tributaries draining segment IV Extended right hepatectomy with MHV excision was planned for an 11·0-cm diameter HCC adherent to the MHV. After clamping the root of the MHV and ligating the right portal vein and right hepatic artery, 1·3 ml ICG was administered intravenously (Figs 4 and 5; Video S2, supporting information). The FI values on the left liver surface increased, providing a clear demarcation between regions with and without venous occlusion (FI values 170 and 220 respectively). The FI values did not increase in ligated portal venous territories (FI value 49). The liver volume of non-veno-occlusive regions (corresponding to left hepatic vein tributaries) was 427 ml (31·1 per cent of TLV). The liver volume of veno-occlusive regions (corresponding to segment IV) was calculated as 296 ml (21·6 per cent of TLV). The transection line was tailored to preserve the MHV branch draining segment IVa, considering the impaired function of veno-occlusive regions. After resection and second intravenous injection of ICG (0·75 ml), fluorescence imaging demonstrated that the FI of segment IVa reached a level similar to that of the left lateral section. Fig. 4 Open in new tabDownload slide Indocyanine green (ICG) fluorescence evaluation of middle hepatic vein (MHV) tributaries draining segment IV. a Contrast-enhanced CT showing an 11·0-cm diameter hepatocellular carcinoma adherent to the MHV (arrowhead). b Gross appearance of the liver. c Regional liver volumes were estimated based on preoperative three-dimensional CT (left image): veno-occlusive regions after division of the MHV (yellow arrowhead), non-veno-occlusive regions (arrow), and ischaemic regions after division of the right hepatic artery and right portal vein (white arrowhead). Gross appearance of the liver after division of the right hepatic artery and right portal vein (middle image). After clamping the MHV and intravenous injection of ICG, fluorescence imaging revealed demarcation among veno-occlusive regions (yellow arrowhead), non-veno-occlusive regions (arrow) and ischaemic regions (white arrowhead) 240 s after ICG injection (right image). Fig. 5 Open in new tabDownload slide Indocyanine green (ICG) fluorescence evaluation of middle hepatic vein (MHV) tributaries draining segment IV. a The liver volume of non-veno-occlusive regions drained by the left hepatic vein was 427 ml (31·1 per cent of total liver volume (TLV)). The MHV tributaries of segment IVa (left image, coloured yellow) and segment IVb (left image, coloured green) were draining a liver volume of 90 ml (6·5 per cent of TLV) and 206 ml (15·0 per cent of TLV) respectively. Accordingly, the transection line (middle image, white dotted line) was tailored to preserve the MHV branch draining segment IVa. Intraoperative ultrasonography revealed the root of the MHV branch draining segment IVa (right image, arrowheads) during transection. b Following resection, fluorescence imaging 240 min after a second ICG injection showed that the fluorescence intensity in segment IVa increased to a level similar to that of non-veno-occlusive regions (right image; arrowheads denote the border between the MHV tributaries of segments IVa and IVb); the gross appearance after extended right hepatectomy is also shown (left image). See also Video S2 (supporting information) Identification of right hepatic vein tributaries among the three right hepatic veins Limited resection with right hepatic vein (RHV) excision was planned for a 1·7-cm diameter HCC in segment VII and adherent to the RHV. There were three RHVs including the RHV trunk, middle RHV and inferior RHV (Fig. S1, supporting information). After clamping the root of the RHV, 1·2 ml ICG was administered intravenously. ICG fluorescence increased in most of the right posterior section owing to drainage through the middle and inferior RHVs (Video S3, supporting information). Resection of segment VII with RHV excision was performed. The histopathological diagnosis was HCC with RHV invasion. ICG fluorescence evaluation of veno-occlusive regions in first and second liver resections Fig. S2 (supporting information) shows fluorescence images during a first and a second liver resection performed at an interval of 9 months in a patient with recurrence of colorectal liver metastases. Initially, extended left hepatectomy with MHV excision was performed without reconstruction of the MHV. The transection line was set to ensure a clear surgical margin and not to leave ischaemic regions. The veno-occlusive regions were not resected after confirming an increase in ICG fluorescence. The patient developed a recurrence 9 months after the first liver resection. Contrast-enhanced CT revealed development of intersegmental venous communication between the divided MHV branches and the RHV. During the second liver resection, ICG was injected intravenously to evaluate the perfusion status of the divided MHV territories. ICG fluorescence imaging visualized no obvious demarcation between the former veno-occlusive and non-veno-occlusive regions, implying similar hepatic perfusion status. The FIVO/FINon ratio increased from 0·83 at the first liver resection to 1·00 at the second. The hypertrophy ratio of the anterior section including venous occlusion (1·06) was comparable to that of the posterior section (1·08). Surgical and short-term outcomes Surgical and short-term outcomes are summarized in Table 3. There were no deaths in hospital or within 30 days. Postoperative complications developed in six patients, including one who underwent endoscopic retrograde cholangiopancreatography for a bile leak (grade IIIa). Table 3 Surgical and short-term outcomes . No. of patients* (n = 21) . Duration of operation (min)† 453 (162–757) Blood loss (ml)† 1175 (95–3407) Duration of inflow occlusion (min)† 92 (17–225) Transfusion requirement† Red blood cell concentrate (ml) 0 (0–1680) Fresh frozen plasma (ml) 0 (0–1200) Maximum tumour size (mm)† 40 (6–110) No. of tumours† 1 (1–7) Morbidity‡ Grade I or II 5§ Grade III or IV 1¶ Death 0 Postoperative hospital stay (days)† 10 (6–84#) . No. of patients* (n = 21) . Duration of operation (min)† 453 (162–757) Blood loss (ml)† 1175 (95–3407) Duration of inflow occlusion (min)† 92 (17–225) Transfusion requirement† Red blood cell concentrate (ml) 0 (0–1680) Fresh frozen plasma (ml) 0 (0–1200) Maximum tumour size (mm)† 40 (6–110) No. of tumours† 1 (1–7) Morbidity‡ Grade I or II 5§ Grade III or IV 1¶ Death 0 Postoperative hospital stay (days)† 10 (6–84#) * Unless indicated otherwise; † values are median (range). ‡ Clavien–Dindo grade14. §Infectious fluid accumulation (2), ileus (2), pneumonia (1); ¶ endoscopic retrograde cholangiopancreatography for bile leak. # Hospital stay prolonged in one patient because of treatment of rectal anastomotic leak. Open in new tab Table 3 Surgical and short-term outcomes . No. of patients* (n = 21) . Duration of operation (min)† 453 (162–757) Blood loss (ml)† 1175 (95–3407) Duration of inflow occlusion (min)† 92 (17–225) Transfusion requirement† Red blood cell concentrate (ml) 0 (0–1680) Fresh frozen plasma (ml) 0 (0–1200) Maximum tumour size (mm)† 40 (6–110) No. of tumours† 1 (1–7) Morbidity‡ Grade I or II 5§ Grade III or IV 1¶ Death 0 Postoperative hospital stay (days)† 10 (6–84#) . No. of patients* (n = 21) . Duration of operation (min)† 453 (162–757) Blood loss (ml)† 1175 (95–3407) Duration of inflow occlusion (min)† 92 (17–225) Transfusion requirement† Red blood cell concentrate (ml) 0 (0–1680) Fresh frozen plasma (ml) 0 (0–1200) Maximum tumour size (mm)† 40 (6–110) No. of tumours† 1 (1–7) Morbidity‡ Grade I or II 5§ Grade III or IV 1¶ Death 0 Postoperative hospital stay (days)† 10 (6–84#) * Unless indicated otherwise; † values are median (range). ‡ Clavien–Dindo grade14. §Infectious fluid accumulation (2), ileus (2), pneumonia (1); ¶ endoscopic retrograde cholangiopancreatography for bile leak. # Hospital stay prolonged in one patient because of treatment of rectal anastomotic leak. Open in new tab Discussion Use of the venous clamp–ICG technique, before parenchymal transection, enabled real-time visualization of three regions with different FI levels. These three regions represented differing hepatic perfusion status during liver resection with excision of hepatic veins: non-veno-occlusive, veno-occlusive and ischaemic regions. This technique provided visual guidance to the surgeons in modifying the liver transection line during surgery. Using the venous clamp–ICG technique, MHV drainage territories were visualized during extended left liver resection and extended right liver resection. The transection line was tailored and/or modified while considering the surgical margin and the extent of venous occlusion. Additionally, portal venous territories were visualized by the absence of fluorescence during clamping or ligating of the left/right portal veins. Ischaemic regions can be visualized by MHV clamping during extended left/right hepatectomy after portal vein embolization. Preoperative 3D CT simulation can visualize the extent of divided hepatic vein territories. However, these virtual images do not completely reflect the actual liver because visualization of small portal and venous branches depends on the quality of CT. Intraoperative ICG fluorescence imaging can be more accurate than preoperative 3D CT simulation because it is based on actual hepatic perfusion status. In the present study, this technique was used to investigate the success or failure of preservation of venous drainage. The surgical procedure for a small tumour adherent to the major hepatic vein root may be challenging. Surgeons must choose between major or minor liver resection, resection or preservation of hepatic veins, and between sacrifice or reconstruction of the hepatic veins. This technique revealed that venous drainage of the right posterior section was not impaired after resection of the RHV because of drainage through the middle and inferior RHVs. Limited resection of segment VII along with RHV excision was selected, and the RHV drainage territories were left as veno-occlusive regions in the remnant liver. Thus, the venous clamp–ICG technique can be of added value when the hepatic veins are involved by large tumours. The technique can enhance the accuracy and safety of complex liver resections including extended major hepatectomy with hepatic vein resection. Doppler ultrasonography, visual inspection and intraoperative portal pressure measurement are other techniques used to evaluate veno-occlusive regions. Doppler ultrasonography can demonstrate the direction of venous flow, but the extent of veno-occlusive regions cannot be visualized. In one study15, 8 per cent of veno-occlusive regions were faintly visualized on the liver surface from the gross appearance and, after temporary hepatic artery clamping, 78 per cent of veno-occlusive regions were clearly visualized. The venous clamp–ICG technique visualized veno-occlusive regions as territories with low FI in all patients, including those with liver cirrhosis and those who underwent preoperative chemotherapy. Intraoperative portal pressure measurement is important to assess hepatic circulation and haemodynamic change16, but cannot be used to identify the extent of veno-occlusive regions. The present authors reported previously that ICG fluorescence imaging visualizes regions with venous occlusion in the remnant liver7, and can be used to assess the function of veno-occlusive regions7, and evaluate regions with and without venous occlusion in transplanted liver grafts after hepatic vessel reconstruction17. Subsequently, two groups18,19 have reported visualization of RHV drainage territories by clamping the RHV root and injecting ICG intravenously. They described fluorescence imaging of temporarily clamped hepatic venous territories as a ‘non-staining area’ or ‘non-fluorescent area’. However, these designations are inaccurate, because the FI of such territories increased7, although it was lower than that of non-veno-occlusive regions. In contrast, temporarily clamped or ligated portal venous territories did not fluoresce. These differences should be clarified when using ICG fluorescence imaging to navigate liver resection. Regions with venous occlusion (veno-occlusive regions, low fluorescence) should be managed differently from regions with portal/arterial occlusion (ischaemic regions, no fluorescence)20. In this study, veno-occlusive region volumes ranged widely from 30 to 458 ml. Short-term outcomes were acceptable. In the patient who underwent repeat liver resection after a 9-month interval, former veno-occlusive regions regained FI values comparable to those of non-veno-occlusive regions. This implies that previous veno-occlusive regions do not always stay congested, but probably become fully functional owing to the development of venous communications. As the perfusion of veno-occlusive regions decreased to 30–40 per cent of that in non-veno-occlusive regions7, functional evaluation of veno-occlusive regions may be important to avoid postoperative liver failure. A drawback of this technique is that, in general, it can be used only once during liver resection. Visualization of tumour fluorescence is hindered after intravenous ICG injection for this technique. Tumour surveillance using ICG fluorescence imaging should be performed before intraoperative ICG injection. Regions with hepatic venous occlusion or portal venous occlusion cannot be visualized successfully when the hepatic veins are incompletely clamped. In future, the functional reserve in the remnant liver including divided portal and hepatic vein territories needs to be investigated. Acknowledgements The authors thank N. Akamatsu, A. Miyata, M. Otani, Y. Ohashi, K. Sugawara, K. Itoh, K. Kawasaki, Y. Suka, M. Yamamoto, T. Ota, N. Senbonmatsu, Y. Shinno and K. Katagiri for acquisition of data and helpful insights. Disclosure: The authors declare no conflict of interest. References 1 Radtke A , Sgourakis G, Sotiropoulos GC, Molmenti EP, Saner FH, Timm S et al. Territorial belonging of the middle hepatic vein in living liver donor candidates evaluated by three-dimensional computed tomographic reconstruction and virtual liver resection . Br J Surg 2009 ; 96 : 206 – 213 . Google Scholar Crossref Search ADS PubMed WorldCat 2 Satou S , Sugawara Y, Tamura S, Kishi Y, Kaneko J, Matsui Y et al. Three-dimensional computed tomography for planning donor hepatectomy . Transplant Proc 2007 ; 39 : 145 – 149 . Google Scholar Crossref Search ADS PubMed WorldCat 3 Hemming AW , Reed AI, Langham MR, Fujita S, van der Werf WJ, Howard RJ. Hepatic vein reconstruction for resection of hepatic tumors . Ann Surg 2002 ; 235 : 850 – 858 . Google Scholar Crossref Search ADS PubMed WorldCat 4 Aoki T , Sugawara Y, Imamura H, Seyama Y, Minagawa M, Hasegawa K et al. Hepatic resection with reconstruction of the inferior vena cava or hepatic venous confluence for metastatic liver tumor from colorectal cancer . J Am Coll Surg 2004 ; 198 : 366 – 372 . Google Scholar Crossref Search ADS PubMed WorldCat 5 Saiura A , Yamamoto J, Sakamoto Y, Koga R, Seki M, Kishi Y. Safety and efficacy of hepatic vein reconstruction for colorectal liver metastases . Am J Surg 2011 ; 202 : 449 – 454 . Google Scholar Crossref Search ADS PubMed WorldCat 6 Makuuchi M , Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy . Surg Gynecol Obstet 1985 ; 161 : 346 – 350 . Google Scholar PubMed OpenURL Placeholder Text WorldCat 7 Kawaguchi Y , Ishizawa T, Miyata Y, Yamashita S, Masuda K, Satou S et al. Portal uptake function in veno-occlusive regions evaluated by real-time fluorescent imaging using indocyanine green . J Hepatol 2013 ; 58 : 247 – 253 . Google Scholar Crossref Search ADS PubMed WorldCat 8 Mise Y , Hasegawa K, Satou S, Aoki T, Beck Y, Sugawara Y et al. Venous reconstruction based on virtual liver resection to avoid congestion in the liver remnant . Br J Surg 2011 ; 98 : 1742 – 1751 . Google Scholar Crossref Search ADS PubMed WorldCat 9 Saito S , Yamanaka J, Miura K, Nakao N, Nagao T, Sugimoto T et al. A novel 3D hepatectomy simulation based on liver circulation: application to liver resection and transplantation . Hepatology 2005 ; 41 : 1297 – 1304 . Google Scholar Crossref Search ADS PubMed WorldCat 10 Urata K , Kawasaki S, Matsunami H, Hashikura Y, Ikegami T, Ishizone S et al. Calculation of child and adult standard liver volume for liver transplantation . Hepatology 1995 ; 21 : 1317 – 1321 . Google Scholar Crossref Search ADS PubMed WorldCat 11 Makuuchi M , Kosuge T, Takayama T, Yamazaki S, Kakazu T, Miyagawa S et al. Surgery for small liver cancers . Semin Surg Oncol 1993 ; 9 : 298 – 304 . Google Scholar Crossref Search ADS PubMed WorldCat 12 Kubota K , Makuuchi M, Kusaka K, Kobayashi T, Miki K, Hasegawa K et al. Measurement of liver volume and hepatic functional reserve as a guide to decision-making in resectional surgery for hepatic tumors . Hepatology 1997 ; 26 : 1176 – 1181 . Google Scholar PubMed OpenURL Placeholder Text WorldCat 13 Ishizawa T , Fukushima N, Shibahara J, Masuda K, Tamura S, Aoki T et al. Real-time identification of liver cancers by using indocyanine green fluorescent imaging . Cancer 2009 ; 115 : 2491 – 2504 . Google Scholar Crossref Search ADS PubMed WorldCat 14 Clavien PA , Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD et al. The Clavien–Dindo classification of surgical complications: five-year experience . Ann Surg 2009 ; 250 : 187 – 196 . Google Scholar Crossref Search ADS PubMed WorldCat 15 Sano K , Makuuchi M, Miki K, Maema A, Sugawara Y, Imamura H et al. Evaluation of hepatic venous congestion: proposed indication criteria for hepatic vein reconstruction . Ann Surg 2002 ; 236 : 241 – 247 . Google Scholar Crossref Search ADS PubMed WorldCat 16 Feng AC , Fan HL, Chen TW, Hsieh CB. Hepatic hemodynamic changes during liver transplantation: a review . World J Gastroenterol 2014 ; 20 : 11 131 – 11 141 . Google Scholar Crossref Search ADS WorldCat 17 Kawaguchi Y , Sugawara Y, Ishizawa T, Satou S, Kaneko J, Tamura S et al. Identification of veno-occlusive regions in a right liver graft after reconstruction of vein segments 5 and 8: application of indocyanine green fluorescence imaging . Liver Transpl 2013 ; 19 : 778 – 779 . Google Scholar Crossref Search ADS PubMed WorldCat 18 Inoue Y , Saiura A, Arita J, Takahashi Y. Hepatic vein-oriented liver resection using fusion indocyanine green fluorescence imaging . Ann Surg 2015 ; 262 : e98 – e99 . Google Scholar Crossref Search ADS PubMed WorldCat 19 Kurihara T , Yamashita YI, Yoshida Y, Takeishi K, Itoh S, Harimoto N et al. Indocyanine green fluorescent imaging for hepatic resection of the right hepatic vein drainage area . J Am Coll Surg 2015 ; 221 : e49 – e53 . Google Scholar Crossref Search ADS PubMed WorldCat 20 Kawaguchi Y , Hasegawa K, Kokudo N, Tanaka N. Should we remove divided hepatic venous territory retaining portal flow? J Am Coll Surg 2016 ; 222 : 211 – 212 . Google Scholar Crossref Search ADS PubMed WorldCat © 2017 BJS Society Ltd Published by John Wiley & Sons Ltd This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model) © 2017 BJS Society Ltd Published by John Wiley & Sons Ltd
TI - Liver transection using indocyanine green fluorescence imaging and hepatic vein clamping
JF - British Journal of Surgery
DO - 10.1002/bjs.10499
DA - 2017-05-18
UR - https://www.deepdyve.com/lp/oxford-university-press/liver-transection-using-indocyanine-green-fluorescence-imaging-and-2sHJYmDj4I
SP - 898
EP - 906
VL - 104
IS - 7
DP - DeepDyve
ER -