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Original Article Ex vivo cholangioscopy in liver grafts: a novel technique to assess the biliary tree during organ preservation and machine perfusion: a experimental non-clinical study
Mark Ly1,2,3,4orcid, Ngee-Soon Lau1,2,4orcid, Joanna Huang1,4orcid, Hayden Ly1orcid, Kasper Ewenson1,4orcid, Nicole Mestrovic1,4orcid, Paul Yousif1,2orcid, Ken Liu2,3,4orcid, Avik Majumdar2,4orcid, Geoffrey McCaughan2,3,4orcid, Michael Crawford1,2,4orcid, Carlo Pulitano1,2,4orcid
Clinical Endoscopy 2025;58(2):303-310.
DOI: https://doi.org/10.5946/ce.2024.099
Published online: March 4, 2025

1Centre for Organ Assessment Repair and Optimisation, Royal Prince Alfred Hospital, Sydney, Australia

2Australian National Liver Transplantation Unit, Royal Prince Alfred Hospital, Sydney, Australia

3Centenary Institute, Sydney, Australia

4Faculty of Medicine and Health, The University of Sydney, Sydney, Australia

Correspondence: Carlo Pulitano 9E Australian National Liver Transplantation Unit, Royal Prince Alfred Hospital, Missenden Rd, Camperdown 2050, NSW Australia E-mail: carlo.pulitano@sydney.edu.au
• Received: April 27, 2024   • Revised: July 1, 2024   • Accepted: July 2, 2024

© 2025 Korean Society of Gastrointestinal Endoscopy

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Background/Aims
    Biliary complications are a leading cause of morbidity after liver transplantation, but can be reduced using real-time assessment of the biliary tree. This study described a novel technique for performing ex vivo cholangioscopy during cold static storage and normothermic machine perfusion (NMP) to assess the biliary tree before liver transplantation.
  • Methods
    Human donor livers, which were considered unsuitable for transplantation, were perfused at 36ºC using a modified commercial ex vivo perfusion system. Ex vivo cholangioscopy was performed using a SpyGlass Discover system. Cholangioscopy was performed during cold static storage and after 12 hours in NMP. Bile duct biopsies and confocal microscopy were performed.
  • Results
    Ex vivo cholangioscopy was performed on eight grafts. During cold static storage, luminal debris was visualized throughout the biliary tree. After 12 hours of reperfusion, the bile ducts appeared hyperemic, heterogeneous, and mottled. Confocal microscopy confirmed perfusion of biliary microvasculature.
  • Conclusions
    We describe the first use of ex vivo cholangioscopy to assess the biliary tree before liver transplantation. This real-time technique can be used to assess biliary trees during cold static storage and NMP. In addition, cholangioscopy-based interventions can be used to better assess intrahepatic bile ducts.
  • Keywords: Biliary tract diseases; Liver transplantation; Organ preservation
Biliary complications are a leading cause of morbidity after liver transplantation and are associated with cellular injury during organ preservation.1-3 It has been suggested that assessment of the biliary tree during organ preservation could reduce the incidence of biliary complications.1,3-5 However, in clinical practice, assessment of the biliary tree during organ preservation remains unfeasible due to the time constraints of liver transplantation.5 As a result, novel real-time techniques, such as cholangioscopy are needed to assess the bile ducts.6
Although cholangioscopy has been proposed as a technique to assess the bile ducts before liver transplantation, it has never been described.6 Direct visualization of the intrahepatic biliary tree can be combined with sophisticated diagnostic tools such as confocal endomicroscopy.7,8 Furthermore, cholangioscopy can also be performed during ex vivo normothermic machine perfusion (NMP) to assess biliary tree perfusion. NMP has generated considerable interest as a novel method for organ preservation and assessment of liver grafts.9-11 In contrast to traditional cold static storage, NMP replicates a near-physiological state and allows assessment of reperfusion injury.10,11 Therefore, performing ex vivo cholangioscopy during NMP could allow real-time assessment of reperfusion injury to the bile ducts.
This study described the first use of cholangioscopy during static cold storage and NMP. Furthermore, we describe the potential applications and benefits of ex vivo cholangioscopy.
Donor livers deemed unsuitable for transplantation, retrieved between March and April 2021 in New South Wales, Australia, were included in this study. As Australia has a centralized national organ procurement organization, the grafts included in this study were declined for transplantation across all Australian transplant units.
Grafts were retrieved using the standard technique and preserved in cold University of Wisconsin solution, as previously described.12 After transport to the Royal Prince Alfred Centre for Organ Assessment Repair and Optimisation, the grafts underwent routine back-table preparation. The vessels and common bile ducts were identified and isolated. A female-to-female luer adaptor (Argon Medical) was placed in the distal common bile duct and secured with a ligature. A luer adaptor was used as an access sheath for the cholangioscope. The liver was then oriented with the porta hepatis directed superiorly and the diaphragmatic surface directed inferiorly for ex vivo cholangioscopy.
At the end of the cold static storage, a cholangioscope (SpyGlass Discover; Boston Scientific) was introduced into the common bile duct (Fig. 1). The irrigation port was connected to a 20 mL syringe filled with room-temperature saline (Fig. 1). Saline was administered to the bile duct lumen to provide intermittent vision. Care was taken to avoid high intraluminal pressure and excess fluid overflow around the cholangioscope. Surgical trainees performed cholangioscopy under the supervision of board-certified hepatobiliary surgeons. No additional training was required. Second-order bile ducts were readily visualized by the trainees in all cases.
After the initial cholangioscopy, the grafts were removed from cold static storage and NMP was performed using a previously described protocol. Briefly, a commercial system (Liver Assist; Organ Assist) was modified by adding a dialysis filter and gas mixer. Livers were perfused at 36ºC and maintained using supportive nutrition and infusions until criteria for hepatocellular death were met. Ex vivo cholangioscopy was repeated in all grafts after 12 hours of NMP to examine the macroscopic evidence of reperfusion injury.
During selected ex vivo cholangioscopies, intrahepatic bile duct biopsies were collected using through-the-scope forceps (SpyBite; Boston Scientific). The tissue specimens were fixed in 10% neutral-buffered formalin, embedded in paraffin, and stained with hematoxylin and eosin. Confocal endomicroscopy was performed using the CellVizio CholangioFlex probe (Mauna Kea Technologies). Fluorescein was added to the perfusate immediately before confocal microscopy to visualize the biliary microvasculature.
Ex vivo cholangioscopy was also performed during ex vivo splitting of the liver. During NMP, the liver was split into left lateral and extended right hemilivers, as previously described. Cholangioscopy was performed during liver splitting to identify the optimal location for bile duct transection. The bile duct was visually transected to ensure a single left duct lumen.
Ethical statements
Ethics approval was obtained from the Sydney Local Health District Ethics Review Committee (X18-0523 and 2019/ETH08964). Consent for research was obtained prior to organ procurement by the national organ donation organisation, DonateLife.
Cholangioscopy was successfully performed on eight grafts during cold static storage and NMP. Donor characteristics are presented in Table 1. Five grafts were obtained from donors after circulatory death donors (DCD). The mean donor age was 51 (±15.6) years and cold ischemic time was 324 (±91.1) minutes. The mean warm ischemic time for DCD grafts was 22 (±6.6) minutes.
Technical development of ex vivo cholangioscopy
Technical modifications were required to allow ex vivo cholangioscopy of the liver grafts (Fig. 1A). First, an access sheath was necessary to minimize intraluminal pressure. We were concerned that the irrigation necessary for lumen visualization might have resulted in high intraluminal pressures. A female-to-female luer adaptor (internal diameter, 4.1 mm) was used as the access sheath. This access sheath allowed the cholangioscope (3.6 mm/10.8 Fr diameter) to pass through and excess fluid to exit the bile duct. Furthermore, we utilized a 20 mL syringe to allow manual and intermittent irrigation of the bile ducts. This allowed the operating endoscopist to carefully control irrigation pressure and flow. Owing to the inverted orientation of the liver, irrigation rarely exceeded 20 mL to achieve adequate visualization. Additionally, cholangioscopy is difficult to perform without an assistant endoscopist. An assistant applied gentle traction to the access sheath (Fig. 1B). This straightened and stabilized the common bile duct, which was required for maneuvering the cholangioscope. The assistant provided intermittent flushing as required.
Cholangioscopic appearance before and during perfusion
During cold static storage, cholangioscopy of all grafts revealed luminal debris throughout the biliary tree (Fig. 2A, C, Supplementary Video 1). The mucosa appeared uniformly dull throughout the biliary tree due to the absence of perfusion. Immediately after perfusion, cholangioscopy revealed significant luminal hyperemia and mucosal heterogeneity. The lumen appeared mottled throughout the intrahepatic and extrahepatic biliary trees (Fig. 2B, 2D, Supplementary Video 1). The cholangioscopic appearance of the grafts during cold storage and after reperfusion is shown in Figures 3 and 4.
Intrahepatic biopsy and intervention
Using the 1.2 mm working channel, cholangioscope-based interventions were performed. Intrahepatic biopsies were performed using the SpyBite forceps. Although these biopsies yielded very large amounts of bile duct tissue, the specimens were comparable to the cross-sectional specimens. Confocal endomicroscopy was performed before and during NMP to evaluate microvascular perfusion. In the absence of perfusion and fluorescein, confocal endomicroscopy did not demonstrate features consistent with histological specimens. Confocal endomicroscopy during NMP confirmed microvascular perfusion of the bile duct (Supplementary Video 2).
Utility of cholangioscopy in clarification of anatomy
Cholangioscopy was useful for assisting bile duct transection during ex vivo liver splitting. During ex vivo liver splitting, cholangioscopy was effectively used to clarify the biliary anatomy and identify the optimal location for bile duct transection. We aimed to transect the left hepatic duct away from any bifurcation to obtain a single lumen. When a single hepatic duct lumen was identified, clamping was performed under cholangioscopic visualization (Fig. 1C, Supplementary Video 3). The hepatic duct was then transected to obtain a single lumen.
Biliary complications are the leading cause of morbidity after liver transplantation and may be reduced by assessing the biliary tree in real time before graft implantation.1,3,6 Real-time assessment of the biliary tree can be used to clarify anatomical variations and identify grafts with severe ischemia-mediated injury. Ischemia is inevitable during organ preservation and transplantation, resulting in a variable degree of biliary tree injury in all grafts.3,6 As a result, histological scores have been developed to evaluate the degree of injury and identify grafts at high risk of biliary complications. However, histological evaluation is impractical in clinical transplantation owing to time constraints. Therefore, real-time techniques are required to assess the biliary trees.
We demonstrated for the first time the technical feasibility of performing ex vivo cholangioscopy during cold static storage and NMP. Technical modifications are needed to perform ex vivo cholangioscopy, such as access sheaths and assistants. These modifications are necessary to overcome the anatomical differences between ex vivo and in vivo cholangioscopy. In the absence of these modifications, attempts to perform ex vivo cholangioscopy to visualize second-order bile ducts are challenging.
This study also investigated the use of cholangioscopy-based interventions, such as biopsy and confocal endomicroscopy. SpyGlass Discover has a 1.2 mm working channel, which allows a variety of interventions. Using SpyBite forceps, focal biopsies of the intrahepatic bile ducts were collected, which were comparable to those of the cross-sectional specimens (Fig. 2F–G). Although complications of the intrahepatic biliary tree can be the most challenging to manage in liver transplantation, assessment of the intrahepatic bile duct remains unfeasible in clinical practice.13 Using cholangioscopy, biopsies of the intrahepatic bile ducts could be safely collected for assessment. However, we recognize that biopsies collected during cholangioscopy yield very limited tissue and may increase the potential for sampling errors compared to cross-sectional specimens. Nevertheless, ischemic injury occurs throughout the entire biliary tree during organ preservation and may be assessed using intrahepatic biopsies.13 Additionally, we also performed confocal endomicroscopy as an alternative to histopathological biopsies. This technique uses a probe-based laser to visualize fluorescence and has commonly been used to diagnose biliary malignancies.7 Confocal endomicroscopy enables the visualization of the pattern of the biliary microvasculature when fluorescein is administered. Therefore, performing this technique during cold static storage, in which the perfusate remains static, was not useful and did not provide a clear image. In contrast, confocal endomicroscopy during NMP provided an image suggestive of microvascular perfusion (Supplementary Video 2). The use of confocal endomicroscopy during NMP illustrates the potential of a multimodal approach to assess the biliary tree by incorporating both ex vivo machine perfusion and cholangioscopy.
Furthermore, we illustrate the potential of using ex vivo cholangioscopy to clarify the anatomy during ex vivo liver splitting. Liver splitting is a technique that enables one liver graft to be transplanted into two recipients.14 The location of hepatic duct transection is a significant issue during liver splitting.15 Surgeons aim to transect the bile duct away from bifurcations and attain a single lumen for anastomosis. Clarifying the biliary anatomy ex vivo before bile duct transection reduces biliary complications.15
To our knowledge, this is the first study to describe the macroscopic appearance of a biliary tree during cold static storage and ex vivo NMP. We observed that debris was common during cold static storage and appeared extensively in the intrahepatic bile ducts. This likely reflects the significant mucosal sloughing and ischemic injury reported in other studies.1,3 In contrast, during ex vivo NMP, bile ducts appeared hyperemic, heterogeneous, and mottled. The clinical significance of our endoscopic findings is unclear, but may reflect reperfusion injury commonly experienced by the bile ducts, as we and other groups have reported.1,3,16 These endoscopic findings illustrate the natural history of ischemia-reperfusion injury to the bile ducts during donor retrieval and subsequent reperfusion.
Although ex vivo cholangioscopy may not be suitable for routine assessment of grafts owing to the time and logistical constraints of liver transplantation, this technique may be particularly useful for the assessment of marginal grafts on NMP. These high-risk grafts are typically assessed on NMP for 2.5 to 6 hours before acceptance for transplantation.4,10,11,17 Ex vivo cholangioscopy should be performed during NMP to evaluate bile duct reperfusion. However, further clinical studies are required to elucidate whether ex vivo cholangioscopy can be used to assess the biliary viability and predict biliary complications.
Although performing cholangioscopy before liver transplantation offers potential benefits for assessing the biliary tree, we recognize the limitations of this technique. First, cholangioscopy requires additional equipment and resources that may not be available at all transplant centers. Additionally, cholangioscopy carries a potential risk of mechanical injury to the biliary mucosa. The limitations of this study included the small sample size and lack of clinical transplantation. The lack of clinical transplantation prevented us from correlating our assessments with post-transplant biliary outcomes. Nevertheless, this study described the technical modifications required to enable ex vivo cholangioscopy for real-time assessment of the bile ducts.
In conclusion, this is the first study describing the technical feasibility of ex vivo cholangioscopy during static cold storage and NMP. Using ex vivo cholangioscopy, we provide the first macroscopic illustration of bile duct reperfusion. This technique can facilitate real-time assessment of the biliary tree and enable interventions for the intrahepatic biliary tree.

Supplementary Video 1.

Bile duct assessment using ex-vivo cholangioscopy.
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Supplementary Video 2.

Confocal endomicroscopy of intrahepatic bile ducts during normothermic machine perfusion.
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Supplementary Video 3.

Ex-vivo cholangioscopy was performed during liver splitting to identify single point of bile duct transection.
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Supplementary materials related to this article can be found online at https://doi.org/ce.2024.099.
Fig. 1.
(A) A female-to-female luer adaptor is secured to the distal common bile duct to act as a cholangioscope sheath. The sheath allows passage of the cholangioscope and for excess irrigation fluid to freely exit the biliary tree. (B) Cholangioscopy during cold static storage. The assistant is stabilizing the bile duct during cholangioscopy and providing intermittent irrigation. (C) Cholangioscopy is performed during liver splitting to identify a suitable location for transection. The line of biliary transection is indicated by the yellow dotted line.
ce-2024-099f1.jpg
Fig. 2.
Cholangioscopy during cold static storage demonstrating significant debris and mucosal sloughing (red arrows) at the hepatic duct bifurcation (A) and subsegmental ducts (C). Repeat cholangioscopy during ex-vivo normothermic machine perfusion demonstrating hyperaemia and mucosal mottling at the hepatic bifurcation (B) and subsegmental ducts (D). Cross sectional biopsies collected during cold static storage (E) and after reperfusion (F) (×10 magnification, hematoxylin and eosin stain). Mucosal sloughing and ischemic injury (red arrows) can be seen during cold static storage. Reperfusion injury with severe mural stromal necrosis (asterisk) can be seen after reperfusion.
ce-2024-099f2.jpg
Fig. 3.
Ex vivo cholangioscopy of grafts 1 to 4 during cold static storage and post-reperfusion. DCD, donation after circulatory death; DBD, donation after brain death.
ce-2024-099f3.jpg
Fig. 4.
Ex vivo cholangioscopy of grafts 5 to 8 during cold static storage and post-reperfusion. DCD, donation after circulatory death; DBD, donation after brain death.
ce-2024-099f4.jpg
ce-2024-099f5.jpg
Table 1.
Donor demographics
Graft Donor type CIT (min) fWIT (min) Cause of death Reason for discard
1 DCD 305 20 Trauma DCD, age, comorbidities
2 DCD 509 31 Trauma DCD, withdrawal of care to death >30 min
3 DBD 187 NA Cardiac arrest, hypoxic brain injury Comorbidities, medically unsuitable, percutaneous cholecystostomy to control biliary sepsis prior to hypoxic brain injury
4 DBD 430 NA Cerebral edema, multi-organ failure, sepsis Deranged LFTs
5 DCD 430 19 Cardiac arrest, aspiration DCD, age, withdrawal of care to death >30 min
6 DCD 284 29 Hypoxia, respiratory failure DCD, high BMI, comorbidities
7 DCD 274 14 Hypoxic brain injury, cardiac arrest DCD, concurrent DBD donor offer
8 DBD 397 NA Intracranial haemorrhage Poor flush of preservation fluid. Congested on the back-table.

Criteria for acceptance of DCD organs: age <50 years and withdrawal of care to death <30 minutes.

CIT, cold ischemic time (cold flush to ex situ machine reperfusion); fWIT, functional warm ischemic time (systolic blood pressure <50 mmHg to cold flush); DCD, donation after circulatory death; DBD, donation after brain death; NA, not applicable; LFT, liver function test; BMI, body mass index.

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        Ex vivo cholangioscopy in liver grafts: a novel technique to assess the biliary tree during organ preservation and machine perfusion: a experimental non-clinical study
        Clin Endosc. 2025;58(2):303-310.   Published online March 4, 2025
        DOI: https://doi.org/10.5946/ce.2024.099
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      Ex vivo cholangioscopy in liver grafts: a novel technique to assess the biliary tree during organ preservation and machine perfusion: a experimental non-clinical study
      Image Image Image Image Image
      Fig. 1. (A) A female-to-female luer adaptor is secured to the distal common bile duct to act as a cholangioscope sheath. The sheath allows passage of the cholangioscope and for excess irrigation fluid to freely exit the biliary tree. (B) Cholangioscopy during cold static storage. The assistant is stabilizing the bile duct during cholangioscopy and providing intermittent irrigation. (C) Cholangioscopy is performed during liver splitting to identify a suitable location for transection. The line of biliary transection is indicated by the yellow dotted line.
      Fig. 2. Cholangioscopy during cold static storage demonstrating significant debris and mucosal sloughing (red arrows) at the hepatic duct bifurcation (A) and subsegmental ducts (C). Repeat cholangioscopy during ex-vivo normothermic machine perfusion demonstrating hyperaemia and mucosal mottling at the hepatic bifurcation (B) and subsegmental ducts (D). Cross sectional biopsies collected during cold static storage (E) and after reperfusion (F) (×10 magnification, hematoxylin and eosin stain). Mucosal sloughing and ischemic injury (red arrows) can be seen during cold static storage. Reperfusion injury with severe mural stromal necrosis (asterisk) can be seen after reperfusion.
      Fig. 3. Ex vivo cholangioscopy of grafts 1 to 4 during cold static storage and post-reperfusion. DCD, donation after circulatory death; DBD, donation after brain death.
      Fig. 4. Ex vivo cholangioscopy of grafts 5 to 8 during cold static storage and post-reperfusion. DCD, donation after circulatory death; DBD, donation after brain death.
      Graphical abstract

      Fig. 1.

      Fig. 2.

      Fig. 3.

      Fig. 4.

      Graphical abstract

      Ex vivo cholangioscopy in liver grafts: a novel technique to assess the biliary tree during organ preservation and machine perfusion: a experimental non-clinical study
      Graft Donor type CIT (min) fWIT (min) Cause of death Reason for discard
      1 DCD 305 20 Trauma DCD, age, comorbidities
      2 DCD 509 31 Trauma DCD, withdrawal of care to death >30 min
      3 DBD 187 NA Cardiac arrest, hypoxic brain injury Comorbidities, medically unsuitable, percutaneous cholecystostomy to control biliary sepsis prior to hypoxic brain injury
      4 DBD 430 NA Cerebral edema, multi-organ failure, sepsis Deranged LFTs
      5 DCD 430 19 Cardiac arrest, aspiration DCD, age, withdrawal of care to death >30 min
      6 DCD 284 29 Hypoxia, respiratory failure DCD, high BMI, comorbidities
      7 DCD 274 14 Hypoxic brain injury, cardiac arrest DCD, concurrent DBD donor offer
      8 DBD 397 NA Intracranial haemorrhage Poor flush of preservation fluid. Congested on the back-table.
      Table 1. Donor demographics

      Criteria for acceptance of DCD organs: age <50 years and withdrawal of care to death <30 minutes.

      CIT, cold ischemic time (cold flush to ex situ machine reperfusion); fWIT, functional warm ischemic time (systolic blood pressure <50 mmHg to cold flush); DCD, donation after circulatory death; DBD, donation after brain death; NA, not applicable; LFT, liver function test; BMI, body mass index.

      Table 1.

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