Name: a heterotopic mouse model for studying laryngeal transplantation
Uploaded: 2023-01-13T12:30:00
Description: Watch this Scientific Journal Video about A Heterotopic Mouse Model for Studying Laryngeal Transplantation at JoVE.com

We would like to thank Randall Raish for his excellent videography and editing assistance.

This research was performed in compliance with the Mayo Clinic Institutional Animal Care and Use Committee (IACUC). BalbC mice (10-12 weeks old) were used as donors and C57/BL6 mice (10-12 weeks old) were used as recipients because their major histocompatibility complexes, H-2Db and H-2Kb, respectively, are immunologically incompatible, and therefore the immune response to the graft can be further studied. All instruments used during surgery were sterilized (see Supplemental Figure S1 and Supplem...

<ol>
	<li>Strome, M., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Laryngeal+transplantation+and+40-month+follow-up.">Laryngeal transplantation and 40-month follow-up.</a> The New England Journal of Medicine. 344 (22), 1676-1679 (2001).</li><li>Hilgers, F. J. M., Ackerstaff, A. H., Aaronson, N. K., Schouwenburg, P. F., Zandwijk, N. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Physical+and+psychosocial+consequences+of+total+laryngectomy.">Physical and psychosocial consequences of total laryngectomy.</a> Clinical Otolaryngology. 15 (5), 421-425 (1990).</li><li>Heyes, R., Iarocci, A., Tchoukalova, Y., Lott, D. G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Immunomodulatory+role+of+mesenchymal+stem+cell+therapy+in+vascularized+composite+allotransplantation.">Immunomodulatory role of mesenchymal stem cell therapy in vascularized composite allotransplantation.</a> Journal of Transplantation. 2016, (2016).</li><li>Kluyskens, P., Ringoir, S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Follow-up+of+a+human+larynx+transplantation.">Follow-up of a human larynx transplantation.</a> Laryngoscope. 80 (8), 1244-1250 (1970).</li><li>Krishnan, G., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+current+status+of+human+laryngeal+transplantation+in+2017:+A+state+of+the+field+review.">The current status of human laryngeal transplantation in 2017: A state of the field review.</a> Laryngoscope. 127 (8), 1861-1868 (2017).</li><li>Strome, S., Sloman-Moll, E., Wu, J., Samonte, B. R., Strome, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Rat+model+for+a+vascularized+laryngeal+allograft.">Rat model for a vascularized laryngeal allograft.</a> Annals of Otology, Rhinology &amp; Laryngology. 101 (11), 950-953 (1992).</li><li>Lorenz, R. R., Dan, O., Nelson, M., Fritz, M. A., Strome, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Rat+laryngeal+transplant+model:+technical+advancements+and+a+redefined+rejection+grading+system.">Rat laryngeal transplant model: technical advancements and a redefined rejection grading system.</a> Annals of Otology, Rhinology &amp; Laryngology. 111 (12), 1120-1127 (2002).</li><li>Shipchandler, T. Z., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=New+mouse+model+for+studying+laryngeal+transplantation.">New mouse model for studying laryngeal transplantation.</a> Annals of Otology, Rhinology &amp; Laryngology. 118 (6), 465-468 (2009).</li><li>Strome, M., Wu, J., Strome, S., Brodsky, G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=A+comparison+of+preservation+techniques+in+a+vascularized+rat+laryngeal+transplant+model.">A comparison of preservation techniques in a vascularized rat laryngeal transplant model.</a> The Laryngoscope. 104 (6), 666-668 (1994).</li><li>Nocini, R., Molteni, G., Mattiuzzi, C., Lippi, G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Updates+on+larynx+cancer+epidemiology.">Updates on larynx cancer epidemiology.</a> Chinese Journal of Cancer Research. 32 (1), 18-25 (2020).</li><li>Strome, S., Sloman-Moll, E., Wu, J., Samonte, B. R., Strome, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Rat+model+for+a+vascularized+laryngeal+allograft.">Rat model for a vascularized laryngeal allograft.</a> Annals of Otology, Rhinology &amp; Laryngology. 101 (11), (1992).</li><li>Work, W. P., Boles, R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Larynx:+Replantation+in+the+dog.">Larynx: Replantation in the dog.</a> Archives of Otolaryngology-Head and Neck Surgery. 82 (4), 401-402 (1965).</li><li>Birchall, M. A., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Model+for+experimental+revascularized+laryngeal+allotransplantation.">Model for experimental revascularized laryngeal allotransplantation.</a> British Journal of Surgery. 89 (11), 1470-1475 (2002).</li><li>Nakai, K., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Rat+model+of+laryngeal+transplantation+with+normal+circulation+maintained+by+combination+with+the+tongue.">Rat model of laryngeal transplantation with normal circulation maintained by combination with the tongue.</a> Microsurgery. 23 (2), 135-140 (2003).</li><li>Lott, D. G., Dan, O., Lu, L., Strome, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Long-term+laryngeal+allograft+survival+using+low-dose+everolimus.">Long-term laryngeal allograft survival using low-dose everolimus.</a> Otolaryngology-Head and Neck Surgery. 142 (1), 72-78 (2010).</li><li>Lott, D. G., Russell, J. O., Khariwala, S. S., Dan, O., Strome, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Ten-month+laryngeal+allograft+survival+with+use+of+pulsed+everolimus+and+anti-&#945;&#946;+T-cell+receptor+antibody+immunosuppression.">Ten-month laryngeal allograft survival with use of pulsed everolimus and anti-&#945;&#946; T-cell receptor antibody immunosuppression.</a> Annals of Otology, Rhinology &amp; Laryngology. 120 (2), 131-136 (2011).</li><li>Lott, D. G., Dan, O., Lu, L., Strome, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Decoy+NF-&#954;B+fortified+immature+dendritic+cells+maintain+laryngeal+allograft+integrity+and+provide+enhancement+of+regulatory+T+cells.">Decoy NF-&#954;B fortified immature dendritic cells maintain laryngeal allograft integrity and provide enhancement of regulatory T cells.</a> The Laryngoscope. 120 (1), 44-52 (2010).</li></ol>

The incidence and prevalence of laryngeal cancer have increased by 12% and 24%, respectively, during the last three decades, and many of these patients undergo a laryngectomy for treatment10. This procedure significantly worsens a person&#39;s quality of life, and therefore an alternative treatment is desired. Vascularized composite allotransplantation of the larynx can improve a patient&#39;s ability to breathe and speak; however, research is still required before this technique can be utilized c...

For patients suffering from irreparable laryngeal damage or laryngeal cancer, a total laryngectomy is often the only option1. Total laryngectomy leaves patients without the ability to breathe and speak on their own, in addition to experiencing social and psychological distress2. Patients with laryngeal cancer who need a total laryngectomy are excellent potential candidates for laryngeal transplantation. While human laryngeal transplantation in the setting of irreparable laryngeal damage has been performed, allotransplantation of the larynx is currently avoided in these patients due to the fear of tumor recurrence, the possibility of chronic rejection, and donor-derived infections3.&#160;Immunosuppression is the primary cause of these concerns. The dramatic loss of the first partial laryngeal transplant patient due to tumor recurrence after conventional immunosuppressive treatment is evidence that an appropriate immunosuppressive regimen should be devised before further attempts are made for transplantation in laryngeal cancer patients4,5.
To better understand the host immune response to a transplanted larynx, the first laryngeal transplant model in rats was developed in 1992 by Strome, and improvements to the surgical technique were made in 20026,7. Although this model is effective for studying laryngeal transplantation, the lack of rat-specific immunological agents and the higher cost associated with rat models led to the development of a new mouse model for studying laryngeal transplantation in 20098.
The main application of the described technique is to study different immunosuppressive drug regimens in laryngeal transplantation. Improving current immunosuppressive therapies may broaden the candidate pool and lead to safe transplantation in cancer patients. The benefits of this mouse model are its cost-effectiveness and the wide availability of immunologic data and reagents.
Teams working on immunosuppressive treatment regimens for laryngeal transplantation can use this method to collect a large volume of immunologic data, and different drug regimens can be rapidly tested and compared. Other potential treatment modalities that can modulate the immune response to the transplant, such as stem cell injections, can also be tested using this model. Finally, experiments can be devised to observe long-term systemic effects of laryngeal transplantation by extending the follow-up period.
The technique described here uses end-to-side anastomoses to provide arterial and venous flow to a heterotopic larynx graft. The graft is a laryngotracheoesophageal (LTE) complex comprising the larynx, thyroid glands, parathyroid glands, trachea, and esophagus of the donor, with bilateral carotid arteries and pedicles intact. One donor carotid artery is anastomosed to the recipient carotid artery and provides arterial blood flow, while the other donor carotid artery is anastomosed to the recipient external jugular vein and provides venous blood flow (Figure 1).
Several modifications were made to the surgical technique of the rat model to ensure success in the mouse model. For instance, an inhaled anesthetic agent was used instead of an injectable agent to increase control over the depth of anesthesia and reduce complications. Continuous suturing is used in the arterial-arterial anastomosis in rats; however, due to the smaller size of mouse vessels, this is technically difficult and can cause narrowing of the vessel lumen7. As a result, interrupted sutures are used in the mouse model and result in improved vessel patency. Additionally, in the rat model, the superior thyroid artery (STA) pedicle is dissected out and visualized. Given the smaller size of the STA in mice, this dissection could result in damage to and even transection of the STA. As a result, it is not dissected in the mouse model. Instead, nearby fascia is preserved to ensure that the STA is kept intact.
The major potential pitfalls of this technique include damaging the donor LTE complex pedicles, making an incorrectly sized arteriotomy or venotomy, vessel occlusion at the anastomosis sites, or leaving gaps at the anastomosis sites which may cause bleeding. To avoid these missteps, care must be taken when procuring the donor graft by leaving a cuff of tissue around the STA pedicle. The arteriotomy and venotomy should be large enough to allow blood flow but small enough to prevent leakage. An appropriate number of sutures should be used for the anastomoses to close any gaps, but not too many to occlude the vessels.
If familiarity with the microsurgical techniques is obtained, this procedure can be performed in approximately 3 h. This laryngeal transplantation model can be performed reliably in mice and used to study the host immune response after vascularized composite allotransplantation.

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a heterotopic mouse model for studying laryngeal transplantation

Laryngeal heterotopic transplantation, although a technically challenging procedure, offers more scientific analysis and cost benefits compared to other animal models. Although first described by Shipchandler et al. in 2009, this technique is not widely used, possibly due to the difficulties in learning the microsurgical technique and time required to master it. This paper describes the surgical steps in detail, as well as potential pitfalls to avoid, in order to encourage effective use of this technique.
In this model, the bilateral carotid arteries of the donor larynx are anastomosed to the recipient carotid artery and external jugular vein, allowing for blood flow through the graft. Blood flow can be confirmed intraoperatively by the visualization of blood filling in the graft bilateral carotid arteries, reddening of the thyroid glands of the graft, and bleeding from micro vessels in the graft. The crucial elements for success include delicate preservation of the graft vessels, making the correct size arteriotomy and venotomy, and using the appropriate number of sutures on the arterial-arterial and arterial-venous anastomoses to secure vessels without leakage and prevent occlusion. 
Anyone can become proficient in this model with sufficient training and perform the procedure in approximately 3 h. If performed successfully, this model allows for immunologic studies to be performed with ease and at low cost.

Confirmation of successful transplantation 
Using the protocol described above, it is possible to assess blood flow to the LTE complex by observing the pulsation of the donor carotid artery after removing the vessel clamps. Pulsation is typically visible, and immediate red coloration of the donor artery confirms active blood flow (Figure&#160;4A). If the anastomosis is not effective, the artery will not have pulsation, look partially collapsed, and be pale in color (<st...

Watch this Scientific Journal Video about A Heterotopic Mouse Model for Studying Laryngeal Transplantation at JoVE.com

A Heterotopic Mouse Model for Studying Laryngeal Transplantation

The aim of this manuscript is to describe the microsurgical steps required to perform a heterotopic laryngeal transplant in mice. The advantages of this mouse model compared to other animal models of laryngeal transplantation are its cost-effectiveness and the availability of immunologic assays and data.

Laryngeal heterotopic transplantation, although a technically challenging procedure, offers more scientific analysis and cost benefits compared to other ...

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