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Method Article

Establishing a Swine Model to Study Whole Eye Transplant Dynamic Preservation and Transplantation

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DOI:

10.3791/69179

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November 25th, 2025

 ,  ,  ,  ,  ,  ,  ,  ,  ,  , 
1Center for Engineering in Medicine and Surgery, Massachusetts General Hospital, Harvard Medical School, 2Shriners Children's Boston, 3Plastic Surgery Research Laboratory, Department of Plastic and Reconstructive Surgery, Massachusetts General Hospital, Harvard Medical School, 4Department of Plastic, Reconstructive and Aesthetic Surgery, Hospices Civils de Lyon, 5Department of Plastic, Reconstructive and Aesthetic Surgery, CHU de Rennes, University of Rennes, 6Faculty of Medicine and Health Sciences, University of Antwerp, 7Bioengineering Research Group, Cardiff Metropolitan University, 8Collaboration for the Advancement of Sustainable Medical Innovation, University College London, 9Division of Plastic Surgery Research, Vascularized Composite Allotransplantation Program Development, Cedars-Sinai Hospital

In This Article

Summary

A detailed and reproducible swine whole eye transplant model (WET) is described, from surgical procurement to the initiation of machine perfusion, allowing for the study of WET dynamic preservation in transplantation.

Abstract

The very first human Whole Eye Transplant (WET) has sparked new hope for patients who have lost vision due to major ophthalmic injury, but significant challenges remain to be addressed before vision restoration through WET can become achievable. Among these, one of the most critical challenges is ex vivo preservation. The eyeball, particularly its neural components such as the retina and optic nerve, undergoes rapid and irreversible degeneration within minutes unless proper preservation is ensured. Static cold storage (SCS) remains the gold standard in vascularized composite allotransplantation (VCA) but is not suited to WET ex vivo preservation due to its inability to sufficiently suppress or support metabolism, leading to loss of graft viability and function. Subnormothermic machine perfusion (SNMP) has emerged as a promising alternative to SCS, offering the potential not only to preserve grafts but also to recondition them. Our group has successfully translated SNMP from solid organ transplantation to several VCA models, demonstrating its feasibility and advantages. Herein, we report the application of SNMP to preserve a WET in swine, detailing the anatomical model and preservation protocol. This approach represents a significant step forward in optimizing WET preservation and transplantation techniques.

Introduction

Vascularized composite allotransplants (VCAs) represent a significant advancement in reconstructive surgery, offering unparalleled aesthetic and functional outcomes for patients with complex lesions1,2. However, eyeball-related vision loss remains a major source of impairment in face injuries. The recent first whole eye transplant (WET) has sparked new hope for patients3,4. Although the sight was not regained, functional imaging demonstrated cortical activation in response to light stimulation, and electroretinography (ERG) indicated a blunted but recognizable photoreceptor response to light5. Despite exceptional technical feats, substantial challenges remain to be addressed to make functional WET a clinical reality. The eyeball is highly sensitive to ischemia, and the retina and optic nerve suffer irreversible degeneration within minutes of warm ischemia time (WIT) unless proper oxygenation and pH levels are maintained6. Thus, WET poses specific challenges within the VCA field, and multiple factors must be considered, including both the posterior and anterior segments, as well as extraocular components. In particular, the musculature is critical for achieving successful functional outcomes, as it is highly susceptible to warm ischemia injuries, which are further exacerbated by ischemia-reperfusion7,8. Oxygen deprivation leads to cell damage and the release of damage-associated molecular patterns (DAMPs). Upon reperfusion, these DAMPs activate the recipient's immune system, triggering inflammation and immune cell infiltration. This inflammatory environment accelerates rejection by promoting antigen presentation and T-cell activation9. Alongside overcoming challenges such as optic nerve reconnection, WET will require optimized ex vivo perfusion techniques to prevent damage resulting from WIT or static cold storage (SCS) and eventually achieve vision restoration5,7,9,10,11.

Machine perfusion (MP) is well-established in solid organ transplantation as a method to prevent ischemia-reperfusion injury12,13,14, with subnormothermic machine perfusion (SNMP) demonstrating superior outcomes compared to SCS in various models15,16,17. We have successfully translated SNMP across animal models ranging from rodents18,19 to swine20,21,22 and, recently, nonhuman primates23. SNMP has not only proven its efficacy in preserving grafts for extended durations but has also shown potential in graft reconditioning and warm ischemic injury mitigation, enabling safe replantation up to 24 h following procurement24,25. Due to its ability to partially maintain cell metabolism, SNMP also opens new avenues by transforming the preservation phase into a diagnostic, therapeutic, and preconditioning platform that can be integrated into replantation and transplantation protocols in VCA. We have developed an optimized SNMP protocol specifically tailored for VCAs and applied it to this challenging whole eye transplant scenario.

In this study, SNMP is employed for oxygenated, dynamic organ preservation at ambient temperature (approximately 20 °C). This technique uses a peristaltic pump and oxygenator to circulate and oxygenate the perfusate. A porcine model is utilized, which is highly relevant for studies on WET transplantation and preservation due to its physiological similarities to humans, comparable vessel size, and the unique absence of a lateral orbital wall26,27,28. This feature makes it particularly suitable for ex vivo experiments and allotransplantation studies, as the external carotid artery and the ophthalmic artery are directly connected, allowing the WET to be procured solely via the external carotid artery and jugular veins without requiring intracranial dissection for ex vivo experiments and in vivo orthotopic or heterotopic replantation. Procurement is performed following circulatory death, aligning with donation after cardiac death protocols and enabling a delay in procurement until other solid organs are harvested. This model, therefore, further explores the potential of SNMP in reconditioning highly sensitive grafts following warm ischemia and supports the development of WET preservation techniques within established transplant laboratories that already focus on other organs, adhering to the "3-R" principles of refinement, reduction, and replacement29,30. Moreover, it remains relevant for heart-beating procurement following similar steps. The goal is to establish a reliable preservation model based on the external carotid and jugular pedicles and to assess its feasibility for dynamic preservation. Detailed procedural steps are provided, encompassing graft procurement, preservation, and key aspects of implementing SNMP.

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Protocol

Institutional approval for this study was obtained from the local Institutional Animal Care and Use Committee (protocol #2024N000205). All animal work followed the Animal Research: Reporting of In Vivo Experiments guidelines31 and was in accordance with the US Army Animal Care and Use Review Office recommendations (ACURO)32. All WETs were procured from swine undergoing terminal organ procurement procedures, following the "3-R" principles33. Animals weighing between 30 kg and 50 kg were euthanized by exsanguination after receiving 100 IU/kg of heparin, and left WET grafts were used for experiments. The right WETs served as controls. Organ procurement occurred post-mortem with less than 180 min of warm ischemia. See the Table of Materials for details about all reagents and equipment used in the protocol.

NOTE: Data were recorded in a spreadsheet (e.g., Excel), and statistical analyses were conducted using an appropriate statistical software (e.g., GraphPad Prism). The alpha risk was set at 5% and was two-tailed. For each monitored variable, the mean and standard error of the mean were determined. The Spearman test was used to study correlations between perfusion parameters.

1. Machine perfusion preparation (1 day prior to the experiment)

  1. Set up the machine perfusion system34(see Figure 1).
    1. Assemble the perfusion system components: pump, oxygenator, bubble trap, continuous pressure sensor, and weight sensor.
      NOTE: Tubing length should be kept to the minimum required to assemble all components of the setup. Once assembled, keep in mind that pressure calibration is specific to the system, particularly to the tubing lengths.
    2. Connect the system as a semi-closed recirculating circuit so as to pump the perfusate from the reservoir into the oxygenator, then the graft inflow (carotid artery). The venous outflow drains back into the reservoir (Supplementary Figure 1 and Supplementary Video 1).
    3. Attach the pressure sensor to the inflow tubing.
    4. Place the graft on the three-dimensional (3D)-printed platform positioned on the electronic scale.
    5. Connect both the scale and the pressure sensor to the microcontroller.
    6. Link the microcontroller to the operator's computer for real-time monitoring and continuous data recording.
    7. Get the thermal camera ready for temperature monitoring.
      NOTE: Weight monitoring, as a surrogate for edema formation, is crucial since it serves as an early indicator of graft injury during perfusion35.
  2. Clean the circuit components thoroughly before initiating perfusion and pay special attention to the oxygenator, particularly if it has been used multiple times.
    1. Start by flushing all tubings separately with 70% ethanol, then with sterile deionized water.
    2. Assemble the system and circulate 2 L of sterile deionized water to flush the oxygenator at a flow rate of 50-100 mL/min if it has already been used.
      NOTE: For live animal replantation studies, use a new sterile oxygenator and sterilize all other perfusion components with ethylene oxide (ETO)
  3. Prepare the perfusate solution. For subnormothermic machine perfusion, use a VCA-optimized Steen+ solution24,34,36. In total, use 1.5 L per graft, following the detailed composition reported previously34.
  4. Add sodium hydroxide solution to the perfusate to achieve a pH of 7.5-7.6. Set this initial value deliberately high, as the pH will decrease during circulation when the carbogen mixture (95% oxygen, 5% carbon dioxide) dissolves.
  5. Calibrate the weight and pressure sensors to ensure accurate measurements.
    1. Tare the scale to account for the platform weight.
    2. To precisely measure vascular pressure, calibrate the system according to the catheter gauge and flow rate used: measure the system pressure for each catheter size that may be used at regular flow rate intervals (every 0.5 mL increment, from 0 to 20 mL/min).
    3. During experiments, to calculate the arterial pressure, subtract the calibration pressure from the total pressure that is being measured. The calibration table used in these experiments is provided as an example (Supplementary Figure 2).
      NOTE: Calibration is specific to each setup. Repeat calibration after any change in tubing, oxygenator, or perfusate, as these modifications can alter system pressure.

2. Post-mortem WET procurement

NOTE: To simulate donation after cardiac death and/or post-mortem procurement, the animal should be euthanized according to local IACUC guidelines. Prefer exsanguination to intravenous pentobarbital injection to avoid drug toxicity that could interfere with the study.

  1. Keep the euthanized animal in the prone position. Shave and scrub the head and neck area and place sterile drapes.
    NOTE: The anatomical model is presented in Figure 2, and a step-by-step dissection guide is provided in Supplementary File 1.
  2. Draw the cutaneous markings of the flap.
    1. Ensure the markings consist of a line around the orbit, 2 cm from the orbital rim, and an incision extended 1 cm below the lateral canthus toward the neck.
    2. Carry out the incision with a n°23 scalpel through the skin and subcutaneous tissue down to the bone at the upper and lower aspects of the orbit, including the periosteum. At the anterior and posterior aspects of the flap, ensure the incision reaches the fascial plane.
  3. Begin dissection with the anterior aspect of the orbit using Stevens scissors and an Adson forceps.
    1. Elevate the orbital contents in a subperiosteal plane toward the orbital walls with a periosteal elevator.
    2. Identify and divide structures close to the orbital wall using a n°15 blade scalpel, including the oblique muscle insertions and the orbital venous plexus, which exits the orbit to join the frontal vein.
      NOTE: The frontal vein drains into the facial vein, which can be sacrificed to save time, provided the anastomotic branch with the ophthalmic vein is preserved.
  4. Continue the dissection on the posterior aspect of the orbit. With a scalpel, resect the masseter muscle at its zygomatic insertion, followed by the ascending branch of the mandible with a Liston bone cutter. Disarticulate the condyle manually by externally rotating the mandible fragment.
  5. Divide the orbital ligament extending from the zygomatic process to the frontal bone to access the orbital portion of the temporalis muscle. Resect the temporalis muscle.
  6. With a periosteal elevator, create a subperiosteal tunnel beneath the zygomatic arch toward the anterior orbital margin. Use a reciprocating saw to cut the bone. Identify the ophthalmic artery that is located in the inferolateral portion of the orbital cone beneath the temporalis muscle.
  7. Resect the zygomatic arch and the antero-inferior orbital walls using a rongeur.
    NOTE: These steps provide access to the inferolateral aspect of the orbital cone and its vascular pedicle.
  8. Identify and dissect with fine Stevens scissors and microsurgical forceps both branches of the ophthalmic artery as they enter the orbital contents.
    NOTE: Most vessels (external carotid artery and superficial jugular vein) are located below the mandible, except for the facial vein, which is superficial to the mandible.
  9. After isolating the desired length of the external carotid artery and jugular vein, complete the dissection by sectioning the optic nerve, oculomotor nerves, and the vascular pedicle using a scalpel.

3. Preparation for perfusion

  1. On a side table, dilate the carotid artery using a microsurgical dilator and insert an angiocatheter. Secure the cannulation with 3-0 silk ties.
    NOTE: In this protocol, an 18-G angiocatheter was used for all arteries. If the arterial pedicle is short, care must be taken not to insert the catheter too far to avoid selective cannulation of only one of the two ophthalmic branches. The jugular vein does not need to be canulated unless a closed-loop perfusion system is used, which was not the case in this protocol.
  2. To flush the carotid artery, use a 10 mL syringe mounted with a pressure sensor identical to the one used for the perfusion setup. Use 10 mL of heparin (100 IU units/mL) to wash out the vessels so that the outflow is clear. Stay below 35 ± 5 mmHg, as high pressure can lead to microvascular injuries and perfusion failure.

4. Subnormothermic machine perfusion

  1. Connect the cannulated artery of the graft to the inflow tubing of the machine perfusion system and place the graft into the scale.
  2. Start the pump that is set at 2-4 mL/min.
    NOTE: The perfusion flow and pressure rates depend on the protocol used. For VCA, a stable and low-flow regimen is used to prevent capillary damage and edema formation.
  3. Assess viability parameters at each predefined time point in both inflow and outflow using a 1 mL syringe and analyzing samples with the blood gas system machine (e.g., blood gas metrics [pH, pCO2, pO2, lactates, base excess, bicarbonate], glucose, sodium, potassium, calcium, chloride). This allows us to calculate the metabolic state of the graft according to the equations presented in Table 1.
    NOTE: In this protocol, the perfusion lasts for 18 h, and samples from the inflow and the outflow are taken every hour for the first 6 h and then every 3 h for the remaining 12 h.

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Results

A preliminary feasibility test was conducted over a 6-h period of SNMP, followed by 2 h of normothermic machine perfusion (NMP) with whole blood to assess proper reperfusion of the entire graft and simulate replantation. During the SNMP phase, a steady outflow was observed, and the subsequent whole blood reperfusion simulation demonstrated successful recoloration of the entire graft. The perfusion parameters further confirmed the feasibility of the technique (Supplementary Figure 3).

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Discussion

More than two decades after the first clinical cases, VCA continues to face significant immunological and ex vivo preservation challenges, limiting its widespread availability37. These challenges are even more pronounced in the case of WET, which offers exciting prospects for vision restoration but presents unique obstacles, such as achieving successful optic nerve reconnection, preserving the functionality of both the anterior and posterior segments, and maintaining the integrity of the ...

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Disclosures

Some authors declare competing interests. Drs. Uygun, Lellouch, and Cetrulo have patent applications relevant to this study. Drs. Korkut Uygun and Basak Uygun have a financial interest in and serve on the Scientific Advisory Board for Sylvatica Biotech Inc., a company focused on developing high-subzero organ preservation technology. Competing interests for MGH investigators are managed by the MGB in accordance with their conflict-of-interest policies. All the remaining authors declare no conflict of interest.

Acknowledgements

This work was partially funded by the National Institutes of Health under award No R01AR082825 (BEU), R01EB028782 (KU), DoD RTRP RT240044 (KU, AGL, CLC), Shriners Children's 84308 (YB), and ARPA-H sub-award FY25.1065.001 (CLC), and by the National Science Foundation under Grant No. EEC 1941543 (KU). HO and YB received funding from the Fondation des Gueules Cassées. Support from Société Française de Chirurgie Plastique, Reconstructrice et Esthétique (SOFCPRE, France) to HO and YB is greatly acknowledged.

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Materials

List of materials used in this article
NameCompanyCatalog NumberComments
Adson ForcepsFine Science Tools11019-12Surgical tool
Affinity Pixie Oxygenation SystemMedtronicBBP241Oxygenator
Angiocath (24 G)Becton Dickinson381112Canulation catheter
Bovin serum albuminSigma-AldrichA9647Perfusate component
Calcium chloride dihydrateSigma-Aldrich223506Perfusate component
Carbon Dioxide OxygenAirgasUN3156Carbon Dioxide Oxygen mix gas 
Catheter 24 GDutscher921048Artery canulation
D-(+)-Glucose monohydrateSigma-Aldrich49159Perfusate component
DexamethasoneSigma-AldrichD2915Perfusate component
DextranThermo scientific406271000Perfusate component
Dilator forcepsAROSurgical11.946.1102Surgical tool
Excel MicrosoftSpreadsheet
Heparin sodium injectionEugia Pharma63739-953-25Perfusate component
Humulin Regular Insulin humanLilly0002-8215-01Perfusate component
Hydrocortisone sodium succinatePfizer0009-0011-03Perfusate component
LigaclipEthiconMCS20Surgical vascular clips
Liston bone cutterFine Science Tools16104-19Surgical tool
Magnesium chloride hexa-hydrateSigma-AldrichM9272Perfusate component
MasterFlex L/SCole-Parmer77200-32Roller pump
Microsurgical forcepsFine Science Tools11253-20Surgical tool
Periosteal elevatorAROSurgical46.415.18Surgical tool
Polyethylene glycol 35000Sigma-Aldrich25322-68-3Perfusate component
Potassium chlorideSigma-Aldrich7447-40-7Perfusate component
Pressure Monitor, Portable, PM-P-1Living Systems InstrumentationPM-P-1Pressure sensor
Prism GraphPadv. 10.1.1Statistical analysis software
Radnoti Bubble Trap Compliance ChamberRadnoti130149Bubble trap
RAPIDPoint 500Siemens500Blood Gas System
Reiprocating sawStryker5100-37Surgical tool
RongeurFine Science Tools16002-18Surgical tool
Scalpel blade (n15)Fine Science Tools10015-00Surgical tool
Scalpel blade (n23)Fine Science Tools10023-00Surgical tool
Silk suture 3-0EthiconP683HSuture
Sodium bicarbonateSigma-AldrichS5761Perfusate component
Sodium chlorideSigma-AldrichS9888Perfusate component
Sodium hydroxideSigma-Aldrich72068Perfusate component
Sodium phosphate monobasique dihydrate Sigma-Aldrich71505Perfusate component
Stevens scissorsAROSurgical07.367.13Surgical tool
Syringe 1 mLBD309659Sample procurement
Syringe 10 mLDutscher300912Graft flush
Thermal cameraFlir Onehttps://www.flir.fr/products/flir-one-gen-3/?vertical=condition+monitoring&segment=solutionsPerfusion temperature monitoring
Tubing (n°16)Masterflex13-310-282Machine perfusion set up
Vancomycine hydrochlorideSlate run pharmaceuticals70436-021-82Perfusate component

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Ex Vivo PreservationMachine PerfusionStatic Cold StorageOptic NerveRetina PreservationVascularized Composite AllotransplantationGraft ViabilityTransplantation Techniques
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