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Cross-circulation

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Cross-circulation
SpecialtyCardiac surgery, transplant medicine
UsesOpen-heart surgery, Organ preservation, Bioengineering

Cross-circulation is a medical technique in which the circulatory system of one individual is temporarily connected to and shared with that of another, typically to support or maintain physiological function in cases where one system alone would be insufficient. Initially pioneered in the 1950s by cardiac surgeon C. Walton Lillehei, cross-circulation allowed surgeons to perform open-heart surgery on infants and children before the development of reliable heart-lung machines. More recently, the concept has been adapted to rehabilitate injured donor organs and bioengineer transplantable grafts ex vivo.

History

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Origins in cardiac surgery

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In the early 1950s, open-heart surgery was limited by the lack of extracorporeal circulation technologies. In 1954, Dr. C. Walton Lillehei at the University of Minnesota introduced cross-circulation as a method to provide oxygenated blood to patients undergoing complex intracardiac repairs. In this procedure, the patient's circulation was temporarily connected to that of a healthy donor (often a parent), whose heart and lungs would maintain oxygenation and perfusion for both individuals during surgery.[1] This technique allowed for successful repair of congenital heart defects before the widespread availability of cardiopulmonary bypass machines.[2]

Although revolutionary, cross-circulation in its original form raised ethical and safety concerns due to the risks posed to healthy donors. It was largely replaced by mechanical heart-lung machines by the early 1960s.[3] Nevertheless, it marked a major milestone in the history of cardiac surgery and contributed to the evolution of extracorporeal support systems.

Modern applications in organ rehabilitation

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Beginning in the 2010s, cross-circulation was re-envisioned as a platform to rehabilitate and regenerate donor organs outside the body. Drawing inspiration from the historic role of cross-circulation in cardiac surgery, researchers at Columbia University and Vanderbilt University pioneered a modern adaptation of the technique to support and recover ex-vivo organs using a living swine host as physiologic support.[4][5] In this system, an extracorporeal circuit is established between an ex-vivo organ (e.g., lung, liver) and a swine host, allowing systemic regulation from the host to maintain organ homeostasis. This approach provides dynamic hormonal, immune, and metabolic regulation and support that cannot be replicated by conventional mechanical perfusion systems.[6]

Initial studies led by cardiothoracic surgeon Matthew Bacchetta and biomedical engineer Gordana Vunjak-Novakovic demonstrated normothermic support and preservation of ex-vivo lungs for 4 days[7] and the functional repair of ex-vivo lungs with ischemic, aspiration, or infectious injury that would otherwise be deemed unsuitable for transplant.[4][8] Innovations in cannulation strategies and circuit design were developed to optimize platform safety and scalability.[9] Through durable physiologic support and targeted therapeutic intervention, this platform actively facilitates organ recovery, immune modulation, and functional regeneration.

In later work, researchers extended the technique to human donor organs using xenogeneic cross-circulation, where a swine host served as a systemic ‘xeno-support’ animal for an ex-vivo human donor organ.[10][11] These trailblazing studies garnered the attention of several mainstream media outlets.[12][13] Further studies examined immune interactions within this xenogeneic context, revealing an attenuated immune response and permissive environment for donor organ recovery.[14][15] Additional studies confirmed that the platform enables rehabilitation of donor lungs using xeno-support without triggering hyperacute rejection in a human lung transplantation model, laying the groundwork for clinical translation.[16] The platform has since been refined with advanced ex-vivo organ assessment capabilities, integrating real-time monitoring, functional imaging, and molecular diagnostics to guide intervention and clinical decision-making.[17]

As of the mid-2020s, cross-circulation is emerging as a novel tool for organ recovery.[18]

See also

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References

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  1. ^ Gott, Vincent L.; Shumway, Norman E. (March 2004). "Cross-circulation: a milestone in cardiac surgery". The Journal of Thoracic and Cardiovascular Surgery. 127 (3): 617. doi:10.1016/j.jtcvs.2003.12.028. PMID 15001882.
  2. ^ Lillehei, C. Walton (May 1955). "Controlled Cross Circulation for Direct-Vision Intracardiac Surgery: Correction of Ventricular Septal Defects, Atrioventricularis Communis, and Tetralogy of Fallot". Postgraduate Medicine. 17 (5): 388–396. doi:10.1080/00325481.1955.11708211. ISSN 0032-5481. PMID 14371276.
  3. ^ Stoney, William S. (2009-06-02). "Evolution of Cardiopulmonary Bypass". Circulation. 119 (21): 2844–2853. doi:10.1161/CIRCULATIONAHA.108.830174. ISSN 0009-7322. PMID 19487602.
  4. ^ a b O’Neill, John D.; Guenthart, Brandon A.; Kim, Jinho; Chicotka, Scott; Queen, Dawn; Fung, Kenmond; Marboe, Charles; Romanov, Alexander; Huang, Sarah X. L.; Chen, Ya-Wen; Snoeck, Hans-Willem; Bacchetta, Matthew; Vunjak-Novakovic, Gordana (2017-03-06). "Cross-circulation for extracorporeal support and recovery of the lung". Nature Biomedical Engineering. 1 (3). doi:10.1038/s41551-017-0037. ISSN 2157-846X.
  5. ^ Wu, Wei Kelly; Tumen, Andrew; Stokes, John W.; Ukita, Rei; Hozain, Ahmed; Pinezich, Meghan; O’Neill, John D.; Lee, Michael J.; Reimer, Jonathan A.; Flynn, Charles R.; Talackine, Jennifer R.; Cardwell, Nancy L.; Benson, Clayne; Vunjak-Novakovic, Gordana; Alexopoulos, Sophoclis P. (April 2022). "Cross-Circulation for Extracorporeal Liver Support in a Swine Model". ASAIO Journal. 68 (4): 561–570. doi:10.1097/MAT.0000000000001543. ISSN 1058-2916. PMC 9984766. PMID 34352819.
  6. ^ O'Neill, John D.; Guenthart, Brandon A.; Hozain, Ahmed E.; Bacchetta, Matthew (April 2022). "Xenogeneic support for the recovery of human donor organs". The Journal of Thoracic and Cardiovascular Surgery. 163 (4): 1563–1570. doi:10.1016/j.jtcvs.2021.07.055. PMID 34607726.
  7. ^ Hozain, Ahmed E.; Tipograf, Yuliya; Pinezich, Meghan R.; Cunningham, Katherine M.; Donocoff, Rachel; Queen, Dawn; Fung, Kenmond; Marboe, Charles C.; Guenthart, Brandon A.; O'Neill, John D.; Vunjak-Novakovic, Gordana; Bacchetta, Matthew (April 2020). "Multiday maintenance of extracorporeal lungs using cross-circulation with conscious swine". The Journal of Thoracic and Cardiovascular Surgery. 159 (4): 1640–1653.e18. doi:10.1016/j.jtcvs.2019.09.121. PMC 7094131. PMID 31761338.
  8. ^ Guenthart, Brandon A.; O’Neill, John D.; Kim, Jinho; Queen, Dawn; Chicotka, Scott; Fung, Kenmond; Simpson, Michael; Donocoff, Rachel; Salna, Michael; Marboe, Charles C.; Cunningham, Katherine; Halligan, Susan P.; Wobma, Holly M.; Hozain, Ahmed E.; Romanov, Alexander (2019-05-07). "Regeneration of severely damaged lungs using an interventional cross-circulation platform". Nature Communications. 10 (1): 1985. Bibcode:2019NatCo..10.1985G. doi:10.1038/s41467-019-09908-1. ISSN 2041-1723. PMC 6504972. PMID 31064987.
  9. ^ Guenthart, Brandon A.; O’Neill, John D.; Bacchetta, Matthew (November 2022). "Cannulation Strategies in Ex Vivo Lung Perfusion". ASAIO Journal. 68 (11): e222. doi:10.1097/MAT.0000000000001621. ISSN 1058-2916. PMID 34882646.
  10. ^ Hozain, Ahmed E.; O’Neill, John D.; Pinezich, Meghan R.; Tipograf, Yuliya; Donocoff, Rachel; Cunningham, Katherine M.; Tumen, Andrew; Fung, Kenmond; Ukita, Rei; Simpson, Michael T.; Reimer, Jonathan A.; Ruiz, Edward C.; Queen, Dawn; Stokes, John W.; Cardwell, Nancy L. (July 2020). "Xenogeneic cross-circulation for extracorporeal recovery of injured human lungs". Nature Medicine. 26 (7): 1102–1113. doi:10.1038/s41591-020-0971-8. ISSN 1078-8956. PMC 9990469. PMID 32661401.
  11. ^ Wu, Wei Kelly; Ukita, Rei; Patel, Yatrik J.; Cortelli, Michael; Trinh, Vincent Q.; Ziogas, Ioannis A.; Francois, Sean A.; Mentz, Meredith; Cardwell, Nancy L.; Talackine, Jennifer R.; Grogan, William M.; Stokes, John W.; Lee, Youngmin A.; Kim, Jinho; Alexopoulos, Sophoclis P. (September 2023). "Xenogeneic cross-circulation for physiological support and recovery of ex vivo human livers". Hepatology. 78 (3): 820–834. doi:10.1097/HEP.0000000000000357. ISSN 0270-9139. PMC 10440302. PMID 36988383.
  12. ^ Kolata, Gina (2020-07-13). "In Astounding Test, Scientists Revive Damaged Lungs for Transplant". The New York Times. ISSN 0362-4331. Retrieved 2025-04-09.
  13. ^ Cooney, Elizabeth (2020-07-13). "Connecting donated human lungs to pigs repaired damage to the organs, scientists report". STAT. Retrieved 2025-04-09.
  14. ^ Wu, Wei K.; Stier, Matthew T.; Stokes, John W.; Ukita, Rei; Patel, Yatrik J.; Cortelli, Michael; Landstreet, Stuart R.; Talackine, Jennifer R.; Cardwell, Nancy L.; Simonds, Elizabeth M.; Mentz, Meredith; Lowe, Cindy; Benson, Clayne; Demarest, Caitlin T.; Alexopoulos, Sophoclis P. (2023-03-31). "Immune characterization of a xenogeneic human lung cross-circulation support system". Science Advances. 9 (13): eade7647. Bibcode:2023SciA....9E7647W. doi:10.1126/sciadv.ade7647. ISSN 2375-2548. PMC 10065447. PMID 37000867.
  15. ^ Shishido, Yutaka; Tracy, Kaitlyn M.; Wu, W. Kelly; Cortelli, Michael; Petrovic, Mark; Harris, Timothy R.; Simon, Victoria; Francois, Sean; Tucker, William D.; Petree, Brandon S.; Cardwell, Nancy L.; Ukita, Rei; Demarest, Caitlin T.; Alexopoulos, Sophoclis P.; Shaver, Ciara M. (2024-09-18). "Characterization of Porcine Immunoglobulin Deposition in Human Livers Recovered Using a Xenogeneic Cross-Circulation". ASAIO Journal. doi:10.1097/MAT.0000000000002311. ISSN 1058-2916. PMC 11913748. PMID 39288356.
  16. ^ Tracy, Kaitlyn M.; Harris, Timothy R.; Petrovic, Mark; Cortelli, Michael; Tucker, William; François, Sean; Shishido, Yutaka; Simon, Victoria; Petree, Brandon; Johnson, Carl A.; Wu, Wei K.; Cardwell, Nancy L.; Simonds, Elizabeth; Adesanya, TiOluwanimi T.; Fortier, Avery K. (March 2025). "Lung rehabilitation using xenogeneic cross-circulation does not lead to hyperacute rejection in a human lung transplantation model". The Journal of Heart and Lung Transplantation. doi:10.1016/j.healun.2025.02.1696.
  17. ^ Pinezich, Meghan R.; O’Neill, John D.; Guenthart, Brandon A.; Kim, Jinho; Vila, Olaia F.; Ma, Stephen P.; Chen, Ya-Wen; Hozain, Ahmed E.; Krishnan, Aravind; Fawad, Moeed; Cunningham, Katherine M.; Wobma, Holly M.; Van Hassel, Julie; Snoeck, Hans-Willem; Bacchetta, Matthew (March 2025). "Theranostic methodology for ex vivo donor lung rehabilitation". Med: 100644. doi:10.1016/j.medj.2025.100644. PMID 40154476.
  18. ^ Andrijevic, David; Spajic, Ana; Hameed, Irbaz; Sheth, Kevin N.; Parnia, Sam; Griesemer, Adam D.; Montgomery, Robert A.; Sestan, Nenad (2025-03-20). "Mechanisms and strategies for organ recovery". Nature Reviews Bioengineering. doi:10.1038/s44222-025-00293-7. ISSN 2731-6092.
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