Research ArticleClinical Studies
Open Access

Surgical Administration of Indocyanine Green in Hepatectomy for Improved Bile Leakage Detection

TAKEHIKO HANAKI, KEISUKE GOTO, MASAKI MORIMOTO, YUKI MURAKAMI, TOMOYUKI MATSUNAGA, MANABU YAMAMOTO, NARUO TOKUYASU, TERUHISA SAKAMOTO, TOSHIMICHI HASEGAWA and YOSHIYUKI FUJIWARA
Anticancer Research October 2022, 42 (10) 4787-4793; DOI: https://doi.org/10.21873/anticanres.15983

Abstract

Background/Aim: Biliary fistulas (BFs) following hepatic resection are a complication of concern, and methods to completely prevent BFs after hepatic resection have yet to be developed. Our aim was to study the use of systemically administered indocyanine green (ICG) for preventing bile leakage (BL) from the cut surface of the liver. Patients and Methods: The study sample comprised 26 patients who underwent hepatectomy without ICG (conventional observation group; CO-G) and 23 hepatectomy patients who underwent intraoperative detection of BL using systemically administered ICG (ICG observation group; IO-G). We compared the bilirubin levels in drainage effluent between patients in whom BL from the resected liver was observed using conventional assessment with the naked eye and those in whom ICG leakage was used as an indicator of BL. In the IO-G, we also compared the number of BL spots on the resected plane visible to the naked eye with the number of visible spots on an ICG camera. Results: Three days after surgery, the bilirubin levels in the drainage fluid of the IO-G were significantly lower than those in the CO-G (1.3 vs. 1.9 mg/dl, p=0.019). Two cases (7.7%) of International Study Group of Liver Surgery (ISGLS) grade B biliary fistula occurred in the CO-G, but none in the IO-G. In the IO-G, the number of BL spots detected just after hepatectomy was significantly higher using ICG camera observation than the naked eye observation (0.22 vs. 0.91 spots, p<0.001). Conclusion: Observation with systemically administered ICG can detect BLs with more sensitivity than conventional observation with the naked eye. This enables rapid repair and may prevent biliary fistula.

Key Words

Biliary fistula (BF) is a common complication after hepatic resection. With drainage, it often resolves spontaneously, but can sometimes be intractable (1, 2). Persistent BF can lead to serious complications such as intra-abdominal infection. In 2011, the International Study Group of Liver Surgery (ISGLS) (3) indicated that a diagnosis of post-hepatectomy BF could be made in cases with “a bilirubin level greater than three times the serum bilirubin level that persists for more than three days post-operatively”. ISGLS defines BF after hepatectomy as “a bile accumulation or biliary peritonitis”. The ISGLS BF severity classifications are grade A, no treatment; grade B, treatment other than re-operation; or grade C, re-operation. Although various efforts have been made to reduce the rate of BF, the incidence of BF is still relatively high, ranging from 4-24% (4-6), and Hayashi et al. (7) recently reported an association between intraoperative bile leakage (BL) detection and postoperative BF.

Intraoperative BL testing after hepatectomies is a longstanding practice used to detect bile duct injuries and prevent BFs. A meta-analysis of clinical trials found that the BL test reduces the incidence of BF (8). A study of 101 central hepatectomies reported that BL was identified intraoperatively in 41.6% of patients, postoperative BF was identified in 23.8% of patients despite intraoperative repair, and the incidence of postoperative BF was 5.1% in the remaining group without intraoperative BL (6). These results suggested that the BL test and intraoperative BL detection are important for preventing BFs. However, the test cannot detect BL from those bile ducts that do not communicate with the common bile duct such as Nagano’s type D bile duct (9) or Strasberg’s type C bile duct injuries (10). In addition, the test is hard to perform in patients who have not undergone cholecystectomy alongside hepatectomy, as the catheter used to inject the dye solution into bile ducts cannot be cannulated (9, 11). Therefore, there is a need to develop a new test that is easier to use and that can detect all types of BL in all surgical procedures.

Intra-biliary infusion of indocyanine green (ICG) can be used for observation of the hepatic resection site. However, at the current time in Japan, this is not covered by public health insurance. Fortunately, since 2018, insurance has covered the use of ICG camera observation of the resection area to evaluate hepatic blood flow and determine the demarcation line (12). While using ICG for this purpose in our clinical practice, we noticed that ICG leakage could be observed more sensitively with an ICG camera than with the naked eye after liver resection is complete (Figure 1).

Figure 1.
Figure 1.

Observations of gauze pressed against the section plane of the liver after resection. In normal light with naked eye observation, no yellow bile stains were apparent on the gauze. Fine Glisson’s sheath is visible, but no bile leakage (a). Near-infrared observation showed an indocyanine green fluorescent spot on the same gauze (arrow). The arrowhead indicates the bile leakage site corresponding to the fluorescent contamination on the gauze (b). When leaks were detected, the small bile duct end was sutured (arrowhead) and leak repair confirmed.

Previous studies have established that systemic administration of ICG improves the sensitivity with which bile duct secretion can be detected (13). In this study, we utilized the excretion of ICG into bile after its systemic administration to retrospectively observe whether treatment of BL based on its detection using ICG fluorescence in liver section planes reduces drainage fluid bilirubin levels more than treatment based on conventional BL detection through observation alone. The primary outcome was the presence or absence of a reduction in drainage fluid bilirubin levels in the ICG observation group (IO-G) compared to the conventional observation group (CO-G). In addition, we reviewed surgical videos of IO-G patients and compared the number of BL spots in resection planes that were visible to the naked eye with the number of ICG fluorescence spots visible on an ICG camera.

Patients and Methods

Ethics. This study was conducted in accordance with the tenets of the Declaration of Helsinki 1964 and the ethical standards of our institution and was approved by the Tottori University Ethical Review Board (approval No. 21A081). The need for informed consent was waived by Tottori University Ethical Review Board due to the retrospective nature of the study.

Patient enrollment. The case records of 58 patients who underwent hepatectomy at the Tottori University Hospital between January 2020 and August 2021 were reviewed retrospectively. Of these, 26 were treated without ICG or intraoperative ICG camera observation from January to July 2020. These cases were classified as the CO-G. There were 32 consecutive patients treated with hepatectomy between August 2020 and August 2021; 9 were excluded because ICG was not used intraoperatively. The remaining 23 patients were the IO-G, in whom ICG was administered intraoperatively and ICG camera observation of the liver section plane was performed. Thus, data from a total of 49 patients were analyzed and clinicopathological factors were compared (Figure 2).

Figure 2.
Figure 2.

Study flow chart for conventional observation vs. indocyanine green observation in the detection of bile leakage after hepatectomy. ICG, Indocyanine green.

Data collection. The patients’ clinicopathological data were extracted from the electronic medical records. The data collected were as follows: age, sex, body mass index, American Society of Anesthesiologists physical status, preoperative blood test results, postoperative blood test results, Child-Pugh scores, liver damage grades, operative procedures, operation times, intraoperative blood loss, the weights of resected livers, postoperative total bilirubin in drainage effluent, postoperative hospital stay durations, surgical complications (according to the Clavien–Dindo classification system) (14), BF grades (according to ISGLS grading criteria) (3), the presence or absence of post-hepatectomy liver failure (according to ISGLS criteria) (15), postoperative pathological diagnoses, and degree of fibrosis of the background liver (from F0 to F4 according to the new Inuyama classification) (16). Preoperative blood tests were conducted within the four weeks prior to surgery and measured levels of albumin, aspartate transaminase, alanine transaminase, and total and direct bilirubin, as well as prothrombin time (% and international normalized ratio), activated partial thromboplastin time, and ICG retention rate at 15 min. Bilirubin levels in patients’ postoperative serum and drainage effluent were measured on postoperative day (POD)1 and POD3. In the IO-G, the surgical videos were reviewed and the number of BL spots visible to the naked eye was recorded along with the number of BL spots apparent on the ICG camera.

Data availability. The dataset used and analyzed during the current study is available from the corresponding author on reasonable request.

Indocyanine green administration, fluorescence imaging, and perioperative management. In the IO-G group, 10 mg of ICG was intravascularly administered to assess hepatic blood flow and to establish which areas were to be resected or preserved. For positive fluorescence staining of the area to be resected, ICG was administered via the portal vein. After clamping the Glisson’s sheath, ICG was administered systemically to the area to be resected by a trans-peripheral venous route for negative staining. In all IO-G cases, ICG was administered immediately before the hepatic parenchymal transection when the demarcation line was set. When ICG was administered transportally, the liver parenchymal fluorescence of ICG was observed immediately. When administered systemically via the peripheral vein, it was apparent after 20-30 s. The yellow-green fluorescence of ICG was observed in all cases using the 1588 AIM camera system (Stryker, Kalamazoo, MI, USA). All surgical videos were stored as high-resolution data on the hospital’s central server (Isilon X200, Dell EMC, Hopkinton, MA, USA). After each patient’s hepatectomy was completed, the abdominal cavity was washed with 8,000 ml of saline to ensure hemostasis, and the resected area was examined for BL. Sutures were generally used to stop BL when it was detected. In the IO-G, the number of BL spots was recorded by conventional observation, sutures were applied, and after confirming the cessation of BL under normal observation, ICG observation was performed and the number of ICG leaks was recorded. Again, all leaks were sutured. The same procedure was performed in the CO-G group, but using only naked eye observation to identify BL.

All open or laparoscopic hepatectomies were performed by one surgeon specializing in liver surgery (TaH). During liver resection, the intermittent Pringle’s maneuver was usually performed with ≤15 min of clamping and ≥5 min of de-clamping. In all cases, a closed system drainage tube was placed beside the sectioned plane of the liver before the abdomen was closed. On POD3, drainage bilirubin levels were checked and if there was judged to be no BF, or grade A BF only, the drain was removed. This was possible in most cases. When drainage was difficult due to high bilirubin levels and drainage volumes, patients were judged to be BF grade B or higher. Patients with grade B BF were relieved by drainage control. None of the patients required re-laparotomy.

Statistical analysis. All graphing and statistical analyses were performed using IBM SPSS Statistics for Macintosh, version 27.0 (IBM Corp., Armonk, NY, USA). Continuous data are presented as medians (or means) with ranges, while categorical data as frequencies or percentages. Mann-Whitney U-tests or Student t-tests were used to evaluate differences in continuous variables, and Fisher’s exact tests or chi-square tests were used to evaluate differences in categorical variables. A two-tailed p-value of <0.05 was considered statistically significant.

Results

Patient characteristics. Patient characteristics are summarized in Table I. Of the 49 patients, 18 were men (36.7%) and 31 were women (63.3%). The median age was 69 years. Child-Pugh scores for preoperative liver function were 5 in 42 patients (85.7%), 6 in 6 patients (12.2%), and 8 points in 1 (2.0%) patient. Hepatic resection involved one liver segment (Couinaud classification) or more in 23 patients (46.9%). All patients had a drain placed intraoperatively. Postoperative grade B BFs occurred in two patients (4.1%). No positive cases were identified from drain cultures on either POD1 or POD3. The median length of postoperative hospital stay was 7 days (range=5-190) and there were no cases of post-hepatectomy liver failure or in-hospital mortality. Pathological findings showed 24 hepatocellular carcinoma cases (49.0%), 16 metastatic liver cancer cases (32.7%), 4 intrahepatic cholangiocellular carcinoma cases (8.2%), 4 benign lesion cases (8.2%), and 1 bile duct cancer case (2.0%).

View this table:
Table I.

Baseline patient characteristics (n=49).

Table II provides a comparison of perioperative patient characteristics between the CO-G and IO-G. There were no statistically significant differences in sex, age, body mass index, Eastern Cooperative Oncology Group performance status, American Society of Anesthesiologists physical status, preoperative laboratory data, preoperative liver status, or operative findings, including the type of hepatectomy, operation duration, blood loss, and resected liver weight between the two groups.

View this table:
Table II.

Comparison of clinicopathological features between groups in which bile leakage was detected using either naked eye observation or indocyanine green administration.

Postoperative findings. Table II presents postoperative findings. No significant differences were found in serum bilirubin levels on POD1 and POD3 or drainage fluid bilirubin levels on POD1 between the CO-G and IO-G (1.2 vs. 1.0, 1.2 vs. 1.0 and 0.9 vs. 0.7 mg/dl, respectively) (Figure 3). However, median drainage fluid bilirubin levels were significantly lower in the IO-G than the CO-G on POD3 (1.2 vs. 1.9 mg/dl, p=0.019) (Figure 3b). Grade B BF occurred in 2 cases (7.7%) from the CO-G, while none in the IO-G (p=0.397). The duration of postoperative hospital stay was significantly shorter in the IO-G, with a median of 7 days, compared to 8 days in the CO-G (p=0.016).

Figure 3.
Figure 3.

Bilirubin levels in serum and drainage effluent on the first postoperative day (POD1) and the third postoperative day (POD3). Bilirubin serum levels on POD1 and POD3 were not significantly different between the conventional observation group (CO-G) and the indocyanine green (ICG) observation group (IO-G) (a). On POD3, the bilirubin levels in the drainage fluid were significantly lower in the IO-G than in the CO-G (b). Bars indicate the median values and interquartile ranges. NS, Not significant.

Differences in the methods of observation of liver section plane in the ICG group. We reviewed the intraoperative videos of patients in the IO-G and counted the number of sutured bile or ICG leakage spots on the dissected plane of the liver by naked eye observation, and then by ICG camera observation. The results are shown in Figure 4. Significantly more leaks were detected on the hepatic resection plane by ICG camera than by naked eye observation only (mean 0.22 vs. 0.91 spots, p<0.001).

Figure 4.
Figure 4.

Comparison of the number of bile or indocyanine green (ICG) leakage spots on the hepatic resection plane detected through naked eye observation and with an ICG camera. The number of leakage spots visible in the same liver was significantly higher using the ICG camera than with naked eye observation. Bars indicate the mean values and interquartile ranges.

Discussion

Clinicopathological factors were compared between liver resection cases in which ICG was used intraoperatively for the detection of BL and those in which only naked eye observation was used. Although there was no statistical difference in the occurrence of clinically problematic grade B or higher BFs between the two groups (Table II), the frequency of grade B or higher BFs was reduced in IO-G, and this was supported by a decrease in the bilirubin concentration of drainage fluid on POD3 (Figure 3). The use of ICG to identify BL in hepatic resections as fluorescent spots (Figure 1), which were then sutured, led to a significant decrease in the bilirubin concentration of drainage fluid (Figure 3b).

Previous reports have shown that systemic ICG administration the day before surgery improves the detection of biliary tracts at the time of cholecystectomy (6) and that ICG cholangiography from a tube cannulated into the common bile duct can detect BL (17, 18). However, to the best of our knowledge, this is the first study to demonstrate that systemically administered ICG can contribute to the detection of BL after hepatectomy. Important features of this method for observing leakage of intravascularly-administered ICG are its high sensitivity and its ability to detect BL without connection to the main bile duct, as, for example, in Nagano’s type D bile duct injuries (9), which cannot be detected by conventional methods such as the BL test.

The results of this research should be considered within the context of its limitations. First, this study had a retrospective design with a small number of cases. Second, we did not gather chemical evidence that ICG fluorescence from a resection plane of the liver directly reflects BL, and moreover, we did not find a significant reduction in BF of grade B or higher in the comparison of the two groups. Furthermore, it remains unclear whether neglected BLs may lead to BF formation. A prospective randomized control study with a large sample size is needed to statistically demonstrate a reduction in the incidence of grade B or higher BF after hepatectomy. In such a study, the method of comparison adopted herein, using drainage fluid bilirubin levels, may be useful. We are conducting a prospective study on the detection of BL and changes in drainage fluid bilirubin levels with ICG at hepatectomy, with an ICG prospective study group and a non-ICG historical control group (Japan Registry of Clinical Trials, jRCTs061210043, https://jrct.niph.go.jp/en-latest-detail/jRCTs061210043) (11). Third, the extent of ICG uptake by the hepatocytes and its secretion into the bile ducts is highly dependent on liver function. The dosage of ICG used was within the range covered by public health insurance in Japan, but it is unclear whether the dosage should be set according to liver function. Fourth, we did not directly compare serum bilirubin and drainage fluid bilirubin levels because the primary outcome measure was the difference in drainage fluid bilirubin levels between groups. Prospective studies that include patients with post-hepatectomy liver failure may be necessary to fully validate the usefulness of systemically administered ICG.

In summary, this retrospective study of ICG use for BL detection after hepatic resection indicated that systemically administered ICG can increase BL detection, and thereby reduce BF.

Acknowledgements

The Authors would like to thank Dr. Yusuke Endo and Dr. Hiroshi Sunada (Advanced Medicine, Innovation, and Clinical Research Center, Tottori University Hospital, Yonago) for their valuable statistical advice, and the medical staff at Tottori University Hospital.

Footnotes

  • Authors’ Contributions

    TaH contributed to the conception and design of the study and performed the surgery. KG performed data acquisition. KG, MM, and YM contributed to the analysis and interpretation of data and drafting of the manuscript. TM, MY, NT, TS, ToH, and YF performed critical revision of the manuscript. All authors have read and approved the final manuscript. We confirm that all of us have met the criteria for authorship as established by the ICMJE.

  • Conflicts of Interest

    The Authors declare that they have no competing interests.

  • Received June 23, 2022.
  • Revision received August 11, 2022.
  • Accepted August 26, 2022.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

References

  1. ↵
    1. Jaén-Torrejimeno I,
    2. Latorre-Fragua R,
    3. López-Guerra D,
    4. Rojas-Holguín A,
    5. Manuel-Vázquez A,
    6. Blanco-Fernández G and
    7. Ramia JM
    : Jaundice as a clinical presentation in liver hydatidosis increases the risk of postoperative biliary fistula. Langenbecks Arch Surg 406(4): 1139-1147, 2021. PMID: 33389115. DOI: 10.1007/s00423-020-02070-z
    OpenUrlCrossRefPubMed
  2. ↵
    1. Schnelldorfer T,
    2. Torres VE,
    3. Zakaria S,
    4. Rosen CB and
    5. Nagorney DM
    : Polycystic liver disease: a critical appraisal of hepatic resection, cyst fenestration, and liver transplantation. Ann Surg 250(1): 112-118, 2009. PMID: 19561475. DOI: 10.1097/SLA.0b013e3181ad83dc
    OpenUrlCrossRefPubMed
  3. ↵
    1. Koch M,
    2. Garden OJ,
    3. Padbury R,
    4. Rahbari NN,
    5. Adam R,
    6. Capussotti L,
    7. Fan ST,
    8. Yokoyama Y,
    9. Crawford M,
    10. Makuuchi M,
    11. Christophi C,
    12. Banting S,
    13. Brooke-Smith M,
    14. Usatoff V,
    15. Nagino M,
    16. Maddern G,
    17. Hugh TJ,
    18. Vauthey JN,
    19. Greig P,
    20. Rees M,
    21. Nimura Y,
    22. Figueras J,
    23. DeMatteo RP,
    24. Büchler MW and
    25. Weitz J
    : Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery 149(5): 680-688, 2011. PMID: 21316725. DOI: 10.1016/j.surg.2010.12.002
    OpenUrlCrossRefPubMed
  4. ↵
    1. Yamashita Y,
    2. Hamatsu T,
    3. Rikimaru T,
    4. Tanaka S,
    5. Shirabe K,
    6. Shimada M and
    7. Sugimachi K
    : Bile leakage after hepatic resection. Ann Surg 233(1): 45-50, 2001. PMID: 11141224. DOI: 10.1097/00000658-200101000-00008
    OpenUrlCrossRefPubMed
    1. Sakamoto K,
    2. Tamesa T,
    3. Yukio T,
    4. Tokuhisa Y,
    5. Maeda Y and
    6. Oka M
    : Risk factors and managements of bile leakage after hepatectomy. World J Surg 40(1): 182-189, 2016. PMID: 26159119. DOI: 10.1007/s00268-015-3156-8
    OpenUrlCrossRefPubMed
  6. ↵
    1. Ishii T,
    2. Hatano E,
    3. Furuyama H,
    4. Manaka D,
    5. Terajima H and
    6. Uemoto S
    : Preventive measures for postoperative bile leakage after central hepatectomy: a multicenter, prospective, observational study of 101 patients. World J Surg 40(7): 1720-1728, 2016. PMID: 26902629. DOI: 10.1007/s00268-016-3453-x
    OpenUrlCrossRefPubMed
  7. ↵
    1. Hayashi K,
    2. Abe Y,
    3. Shinoda M,
    4. Kitago M,
    5. Yagi H,
    6. Oshima G,
    7. Hori S,
    8. Wakabayashi T and
    9. Kitagawa Y
    : Clinical impact of intraoperative bile leakage during laparoscopic liver resection. Surg Endosc 35(8): 4134-4142, 2021. PMID: 32780232. DOI: 10.1007/s00464-020-07880-2
    OpenUrlCrossRefPubMed
  8. ↵
    1. Wang HQ,
    2. Yang J,
    3. Yang JY and
    4. Yan LN
    : Bile leakage test in liver resection: a systematic review and meta-analysis. World J Gastroenterol 19(45): 8420-8426, 2013. PMID: 24363535. DOI: 10.3748/wjg.v19.i45.8420
    OpenUrlCrossRefPubMed
  9. ↵
    1. Nagano Y,
    2. Togo S,
    3. Tanaka K,
    4. Masui H,
    5. Endo I,
    6. Sekido H,
    7. Nagahori K and
    8. Shimada H
    : Risk factors and management of bile leakage after hepatic resection. World J Surg 27(6): 695-698, 2003. PMID: 12732991. DOI: 10.1007/s00268-003-6907-x
    OpenUrlCrossRefPubMed
  10. ↵
    1. Strasberg SM,
    2. Hertl M and
    3. Soper NJ
    : An analysis of the problem of biliary injury during laparoscopic cholecystectomy. J Am Coll Surg 180(1): 101-125, 1995. PMID: 8000648.
    OpenUrlPubMed
  11. ↵
    1. Hanaki T,
    2. Tokuyasu N,
    3. Sakamoto T and
    4. Fujiwara Y
    : Hepatectomy guided by indocyanine green fluorescent imaging for visualizing bile leakage (with video). Clin Case Rep 10(6): e05942, 2022. PMID: 35662771. DOI: 10.1002/ccr3.5942
    OpenUrlCrossRefPubMed
  12. ↵
    1. Morimoto M,
    2. Taniguchi K,
    3. Yamamoto O,
    4. Naka T,
    5. Sugitani A and
    6. Fujiwara Y
    : Evaluation of blood supply with indocyanine green fluorescence in resection for concurrent gastric and pancreatic cancer: a case report. Yonago Acta Med 64(1): 133-136, 2021. PMID: 33642914. DOI: 10.33160/yam.2021.02.017
    OpenUrlCrossRefPubMed
  13. ↵
    1. Matsumura M,
    2. Kawaguchi Y,
    3. Kobayashi Y,
    4. Kobayashi K,
    5. Ishizawa T,
    6. Akamatsu N,
    7. Kaneko J,
    8. Arita J,
    9. Kokudo N and
    10. Hasegawa K
    : Indocyanine green administration a day before surgery may increase bile duct detectability on fluorescence cholangiography during laparoscopic cholecystectomy. J Hepatobiliary Pancreat Sci 28(2): 202-210, 2021. PMID: 33091224. DOI: 10.1002/jhbp.855
    OpenUrlCrossRefPubMed
  14. ↵
    1. Dindo D,
    2. Demartines N and
    3. Clavien PA
    : Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2): 205-213, 2004. PMID: 15273542. DOI: 10.1097/01.sla.0000133083.54934.ae
    OpenUrlCrossRefPubMed
  15. ↵
    1. Rahbari NN,
    2. Garden OJ,
    3. Padbury R,
    4. Brooke-Smith M,
    5. Crawford M,
    6. Adam R,
    7. Koch M,
    8. Makuuchi M,
    9. Dematteo RP,
    10. Christophi C,
    11. Banting S,
    12. Usatoff V,
    13. Nagino M,
    14. Maddern G,
    15. Hugh TJ,
    16. Vauthey JN,
    17. Greig P,
    18. Rees M,
    19. Yokoyama Y,
    20. Fan ST,
    21. Nimura Y,
    22. Figueras J,
    23. Capussotti L,
    24. Büchler MW and
    25. Weitz J
    : Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery 149(5): 713-724, 2011. PMID: 21236455. DOI: 10.1016/j.surg.2010.10.001
    OpenUrlCrossRefPubMed
  16. ↵
    1. Ichida F,
    2. Tsuji T,
    3. Omata M,
    4. Ichida T,
    5. Inoue K,
    6. Kamimura T,
    7. Yamada G,
    8. Hino K,
    9. Yokosuka O and
    10. Suzuki H
    : New Inuyama classification; new criteria for histological assessment of chronic hepatitis. International Hepatology Communications 6(2): 112-119, 2019. DOI: 10.1016/s0928-4346(96)00325-8
    OpenUrlCrossRef
  17. ↵
    1. Kaibori M,
    2. Ishizaki M,
    3. Matsui K and
    4. Kwon AH
    : Intraoperative indocyanine green fluorescent imaging for prevention of bile leakage after hepatic resection. Surgery 150(1): 91-98, 2011. PMID: 21514613. DOI: 10.1016/j.surg.2011.02.011
    OpenUrlCrossRefPubMed
  18. ↵
    1. Sakaguchi T,
    2. Suzuki A,
    3. Unno N,
    4. Morita Y,
    5. Oishi K,
    6. Fukumoto K,
    7. Inaba K,
    8. Suzuki M,
    9. Tanaka H,
    10. Sagara D,
    11. Suzuki S,
    12. Nakamura S and
    13. Konno H
    : Bile leak test by indocyanine green fluorescence images after hepatectomy. Am J Surg 200(1): e19-e23, 2010. PMID: 20637329. DOI: 10.1016/j.amjsurg.2009.10.015
    OpenUrlCrossRefPubMed
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Surgical Administration of Indocyanine Green in Hepatectomy for Improved Bile Leakage Detection
TAKEHIKO HANAKI, KEISUKE GOTO, MASAKI MORIMOTO, YUKI MURAKAMI, TOMOYUKI MATSUNAGA, MANABU YAMAMOTO, NARUO TOKUYASU, TERUHISA SAKAMOTO, TOSHIMICHI HASEGAWA, YOSHIYUKI FUJIWARA
Anticancer Research Oct 2022, 42 (10) 4787-4793; DOI: 10.21873/anticanres.15983
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