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20Q: Auditory Biotechnologies - Finding Their Way to the Clinic

20Q: Auditory Biotechnologies - Finding Their Way to the Clinic
Rebecca M. Lewis, AuD, PhD
July 10, 2023

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From the Desk of Gus Mueller

Gus-mueller-contributing-editor

You’ve probably noticed that each year we see more and more written about biotechnologies that are related to the auditory system—certainly increasingly popular in the lay press. For example, just last month we saw that Sensorion, a French biotechnology company specializing in hearing loss disorders, announced promising preliminary results from its Phase 2a clinical trial of SENS-401 for residual hearing preservation following cochlear implantation. The news release stated “Preliminary results demonstrated 100% patients treated with SENS-401 showed presence of SENS-401 in perilymph at therapeutic concentrations, confirming that the oral presentation of SENS-401 passed through the labyrinth barrier to the cochlea.”

On the other hand, back in February of this year, the news from Frequency Therapeutics, Inc., a regenerative medicine company located in Massachusetts, wasn’t so good. Their press release read: “Data showed no statistically meaningful difference at day 90 between those administered FX-322 versus those receiving placebo in the proportion of individuals that demonstrated an improvement in speech perception. There were also no measurable improvements observed in any of the study’s secondary endpoints . . . The Company will now discontinue the FX-322 development program.” Not surprisingly, their stock is now trading at ~6% of the January high.

Those are only two examples. There is a lot going on in the area of auditory biotechnologies, and fortunately we have an expert with us this month to tell us all about it. Rebecca M. Lewis, AuD, PhD, Chief of Audiology and assistant professor in the Department of Otolaryngology-Head and Neck Surgery, University of California, San Francisco. Dr Lewis’s research background includes stops at the Eaton Peabody Lab at Massachusetts Eye and Ear Infirmary and Walter Reed National Military Medical Center. 

Dr. Lewis is an associate editor of Frontiers in Audiology and Otology, serves as the Scientific Grants Project Officer for the American Tinnitus Association, Co-Chair for the External Relations Committee of the Association for Research in Otolaryngology, and is Chair of the Academy of Audiology’s American Board of Audiology.

I think you’ll find in reading this excellent 20Q, that Becky’s unique skillset of both a researcher of biotechnologies and a clinical audiologist, are reflected in her insights and perspectives on this important topic.

Gus Mueller, PhD
Contributing Editor

Browse the complete collection of 20Q with Gus Mueller CEU articles at www.audiologyonline.com/20Q

20Q: Auditory Biotechnologies - Finding Their Way to the Clinic

Learning Outcomes 

After reading this article, professionals will be able to:

  • Identify and describe various biotechnologies being researched to treat sensorineural hearing loss, and differentiate between their mechanisms of action in targeting different cellular deficits, including cochlear implants, hair cell regeneration, otoprotective agents, and spiral ganglion neuron regeneration.
  • Evaluate and compare different approaches to otoprotective strategies and hair cell regeneration in the inner ear, including gene therapy, small molecules, drug-like molecules, stem cells, and more, and discuss their potential for restoring hearing in patients with sensorineural hearing loss.
  • Assess and analyze the potential psychosocial and neural degeneration implications of supporting a patient’s pursuit of different hearing restoration technologies of today, such as cochlear implants, while weighing the potential outcomes of hearing restoration technologies of tomorrow, such as hair cell regeneration.
Lewis headshot
Rebecca M. Lewis

1. I hear that you’re an audiologist who, among other things, happens to have a background in auditory biotechnologies. It sounds like an interesting field, but to be honest, I'm not entirely sure exactly what that all entails. Can you tell me a little more about this area and why we should care about it?

Absolutely, one of my favorite things to talk about! Auditory biotechnologies include a range of innovative therapies and technologies designed to prevent, treat, and restore hearing function. These include protective therapies aimed at preventing hearing damage, as well as restorative therapies that can be administered after damage and hearing loss have already occurred. Some examples include hair cell regeneration (Oesterle et al., 2020), restoration of synapses that connect inner hair cells to the spiral ganglion neurons (Wan et al., 2021), regeneration and axonal outgrowth of spiral ganglion neurons (Schmidbauer et al., 2023), otoprotective agents to be delivered along with an ototoxic agent known to damage structures of the inner ear (Wolff et al., 2023), and more.

2. Are these commonly used for patient treatment?

These biotechnologies are still relatively new and are mainly being developed and tested in research settings, with rare opportunities for current clinical use (according to most recent conversations with other leaders in the field). However, with ongoing clinical trials and advancements in technology, these therapies hold great promise for improving audiological care in the future. As audiologists, however, I believe that it's important for us to stay informed about the latest developments in auditory biotechnologies to ensure that we can provide our patients with the best guidance possible. This may include discussing these technologies with patients who are interested in pursuing audiologic care, as well as staying up-to-date with the latest research and developments in the field.

3. Can we start by talking through the restorative therapies today? What types of therapies are currently in the works?

Certainly – restorative therapies are surely a hot topic among patient populations today as these folks have already sustained sensorineural hearing loss and are looking for ways to improve their hearing beyond what today’s hearing devices (hearing aids and cochlear implants) can offer. As we all know, hearing devices do not fully restore hearing; individuals who have experience with hearing aids or cochlear implants can attest to their limitations firsthand (Goudey et al., 2021).

Audiology patient populations that would be most immediately impacted by the introduction of these restorative technologies would generally be individuals who are candidates for cochlear implants. As you know, people who are candidates for cochlear implants present with moderately-severe to profound hearing loss in addition to decreased word recognition scores when stimuli are presented at an audible level above their thresholds. Thinking through the cellular deficits associated with that degree of hearing loss helps you think about what types of restoration would be needed for these folks.

4. Maybe you could help me?

Sure. The first therapy that comes to mind for folks in the cochlear implant candidate pool is hair cell regeneration, my personal favorite! Inner hair cells are a critical sensory cell that allow the small and rapid movements in fluid in the cochlea to be translated into neural information that is sent along to the auditory nerve and up to the brain. Check out a review by Fettiplace (2017) for a much more detailed review of inner hair cell function, down to the level of the critical MET channels! To restore a significant portion of patient’s audibility, inner hair cells would be one area of focus, as the inner hair cells are responsible for receiving the signal and sending this along to auditory neurons, continuing up the brainstem and with the signal finally being “heard” once it reaches the auditory cortex in the brain.

5. What about the outer hair cells?

Right, those are critical to restoring normal hearing sensitivity as well — you can’t just regenerate inner hair cells alone to achieve the ultimate goal of complete hearing restoration. Calling back to our foundational knowledge of hearing science, outer hair cells act as active amplifiers that amplify low-level sound signals, making it easier for the inner ear to detect and process them (and by the way, the Fettiplace review also includes information about outer hair cells). Outer hair cell motility (contraction and relaxation of the cell) also helps to sharpen the tuning of the cochlea, which improves the precision of hearing. This mechanism is known as the "cochlear amplifier" and is a critical component of the normal hearing process. In order to regenerate outer hair cells successfully, this motility would need to be restored as well; although progress has been made, this active process has proven to be more challenging to replicate after the original cell populations have been damaged. (For example, check out this study by Heuermann that shows that many regenerated hair cells have characteristics of both inner and outer hair cells.)

6. How would you start regenerating these cell types in the cochlea?

Cochlear implant surgeries allow for direct access to the cochlea, but we know that the process of placing the implant array carries the risk of sacrificing any remaining hair cells. Using a similar approach as a cochlear implant surgery, placing a stiff structure like an electrode array into the cochlea, will therefore likely be insufficient to regenerate hair cells because we need to encourage growth and development in an already-damaged structure – adding more damage to that structure would certainly damper our outcomes. That's why scientists are exploring various approaches to hair cell regeneration that can be customized to suit each patient's unique requirements.

7. There is more than one approach?

Yes, generally speaking, there are at least three different strategies that one could use to regenerate these structures: gene therapy, small molecules, and stem cells. (Meanwhile, the field of taste and smell disorders discuss similar strategies in a review by Mainland, 2020).

Gene therapy involves introducing specific genes into the inner ear to activate the natural regenerative capacity of the cellular population of this structure. To regenerate hair cells, the most promising cell population to target would be the supporting cells, which have the proper location in the inner ear as well as a variety of genetic markers that would allow us to specifically target those cells as a regenerative target. You can take a look at a recent interesting study from Ishibashi and colleagues at NIDCD about one particular gene therapy that uses an adeno-associated virus to deliver the gene therapy to the inner ear, and how the immune response of the inner ear may affect the success of that gene therapy.

Another method involves using small molecules or drugs that stimulate hair cell growth and differentiation in the inner ear. These molecules can be delivered into the cochlea using minimally invasive surgery or applied topically to the ear canal with special gel-like formulas to assist with transferring the appropriate molecules to the ear. Exosomes, for example, are one example of a small extracellular membrane particle that could potentially serve as a drug delivery tool to the inner ear – see a review by Mittal and colleagues from 2021 for more details.

8. You mentioned that stem cells also are a possibility?

Use of stem cells and biomaterials would require delivering a rather large piece of material to the inner ear. The larger the material delivered to the inner ear, the greater likelihood there is for that material to have difficulty reaching the intended location in the inner ear. For that reason, gene therapy and small molecule delivery mechanisms seem to be the most promising approaches at this time. However, each of these approaches have their own limitations – especially in inner ears that have substantial cellular and structural damage (like our patients who are candidates for cochlear implants).

Ultimately, the specific approach to hair cell regeneration will depend on the patient's individual needs, as well as the severity and type of their hearing loss. This field of research is filled with potential avenues for future development, and we are working tirelessly to identify safe and effective ways to restore hearing function in individuals with sensorineural hearing loss.

9. Small molecules or drugs that stimulate hair cell growth and differentiation in the inner ear sound pretty promising – like popping a pill to cure your hearing loss?

Hmm, it’s not quite that simple, unfortunately. In fact, when a systemic therapy (like using an orally-delivered pharmaceutical) is used in animal studies, the outcome is not only poor in terms of the number of hair cells ultimately regenerated, but the animals also suffer from extreme toxicity, which can result in death depending on the therapy delivered. The molecular and cellular pathways that are called upon to regenerate these structures are pretty ubiquitous throughout the human body; as a result, the therapy has to be targeted to the inner ear alone to ensure side effects are minimized and to maintain human safety.

10. What’s the alternative approach?

We could consider using a locally-delivered therapy (through transtympanic injection, for example), however, a significant challenge remains: ensuring that the therapy travels to the appropriate part of the cochlea, where you want hair cells to be regenerated. There are research groups dedicated to this exact question, of designing the small molecules that can transport the intended therapy to the appropriate location of the organ of Corti to begin differentiating new hair cells. 

11. Would you say that gene therapy is a better option for hair cell regeneration compared to other approaches?

It depends on the nature of cellular damage that the patient has experienced. Gene therapy relies on the remaining cellular populations in the inner ear to stimulate the growth of new hair cells. For patients who have lost hair cells due to ototoxicity, gene therapy could be a promising option as their supporting cell populations are more likely to be intact and able to convert into hair cells. However, for patients who have experienced noise-induced hearing loss, gene therapy may not be as effective. Exposure to loud noise can damage both hair cells and the surrounding supporting cells, making it challenging to stimulate the growth of new hair cells using gene therapy alone. In these cases, it’s possible that stem cells or other biomaterials may be needed to build a scaffolding upon which new cells can grow. For more information, readers can take a look at the recent 2023 review by Chou and Hsu, which discusses a particular strategy that allows for stem cells to be developed using a patient’s own cell samples.

Overall, the choice of approach for hair cell regeneration will depend on the individual patient's needs and the nature of their hearing loss. As we continue to make progress in this field of research, we hope to identify safe and effective treatments that can help restore hearing function for a broad range of patients.

12. We’ve talked a bit about how these therapies would be delivered, but what is actually causing the change?

We do know that there are certain molecules and proteins that have been shown to truly drive this regenerative process forward. Let’s focus on the genes that have been evaluated over the last few decades – there are some standout candidates that will likely play a role in future hair cell regeneration strategies.

I’ll start with Atoh1, which is a gene that is critical for development and function of hair cells in the inner ear. (Readers can check out Zheng & Gao 2000 and Bermingham et al., 2001 for those data.) As a transcription factor, it has the power to modulate the response of many, many other genes – meaning that they can control which genes are turned on or off. They can do this by binding to specific regions of DNA and regulating the expression of nearby genes.

You can think of DNA as a library, with each gene representing a different book. The transcription factor is like a librarian that helps to decide which books are available for reading. When a transcription factor binds to a specific region of DNA, it can either promote or inhibit the expression of the gene that is located nearby.

In the case of Atoh1, it works by binding to specific genes that are involved in the development and maintenance of hair cells. By regulating the expression of these genes, Atoh1 can promote the production of new hair cells which may be able to replace damaged or lost hair cells in the cochlea.

13. Wow, that Atoh1 is powerful! Why can’t we just stick some Atoh1 into someone’s cochlea and call it a day?

Indeed, Atoh1 is a powerful gene that plays an important role in the development of hair cells in the inner ear. However, the process of regenerating hair cells in the cochlea is more complicated than just adding more Atoh1 to the mix. The human body has a complex system of checks and balances that regulate the expression and function of Atoh1, as well as other factors that are involved in hair cell development.

For example, the notch signaling pathway is a well-known inhibitor of Atoh1 expression. This pathway can reduce or eliminate hair cell growth by preventing Atoh1 expression.

14. “Notch signaling pathway?” Never heard of it.

The notch signaling pathway is just another way for cells to communicate with one another. Let’s use another metaphor to incorporate the notch signaling pathway with our understanding of Atoh1: a team of workers repairing a damaged building.

The notch signaling pathway acts like a supervisor who identifies the damaged areas of the building and communicates with the repair workers. Similarly, the damaged hair cells send a signal through the notch pathway to communicate with supporting cells.

Atoh1 acts like a specialized repair worker who has necessary skills to fix the damaged parts of the building. Atoh1, as that powerful transcription factor, helps the supporting cells differentiate into new hair cells, which is essential for repairing the damaged inner ear.

Just as the supervisor and repair workers need to work together to fix the building, the notch signaling pathway and Atoh1 need to work together for successful hair cell regeneration. The notch signaling pathway signals the supporting cells to differentiate, and Atoh1 helps these cells become new hair cells to repair the damaged inner ear, just as the supervisor and repair workers work together to fix the building.

15. Okay, thanks for the explanation—let’s go on.

As I was saying, if we can inhibit the notch signaling pathway (or using our earlier metaphor, tell the supervisor that we need some resources to create more hair cells), then Atoh1 expression can increase and promote more hair cell growth. There are also various growth factors that can affect Atoh1 function in a similar way to the notch pathway. So, the fate of a cell that is targeted for hair cell differentiation is not just determined by Atoh1 alone, nor by the notch signaling pathway alone. It's more like a "voting process" where the input from Atoh1 and many other signaling pathways are weighed before a cell can differentiate into a hair cell. Although Atoh1 gene therapy is a promising approach for stimulating hair cell regeneration, researchers are still working to better understand the complex interplay between various factors involved in hair cell regeneration. There’s a great review by Shibata and colleagues from 2020 that readers can check out if they’re interested in learning more about the basics of Atoh1 and notch signaling as it relates to hair cell regeneration.

I should also mention that, only a few days ago, investigators (Quan and a large team of colleagues) at Massachusetts Eye and Ear and Harvard Medical School published a promising breakthrough using Notch along with other signaling pathways in an animal model, which showed newly generated hair cells in an adult mouse cochlea using drug-like molecules. That’s a big step forward!

16. That’s fantastic that academics are continuing to evaluate different avenues that could work well in future clinical trials. Can you tell me about any companies making progress in the auditory biotechnologies field, and how are they approaching the development of these technologies?

While there are a handful of companies that focus on auditory biotechnologies, only few have made meaningful progress in human studies so far. However, some companies are finding success by including protective agents in their product portfolios instead of relying on restorative therapies alone. Decibel Therapeutics is one such company that presented promising data for their auditory protective agent, DB-020, at the Association for Research in Otolaryngology MidWinter Meeting earlier this year (Wolff et al., 2023). DB-020 is a locally administered product (via transtympanic injection) designed to protect patient ears from cisplatin-induced ototoxicity, which can cause hearing loss during cancer treatment.

The study included individuals who were already undergoing cisplatin treatment and suffered from bilateral ototoxic-related hearing loss, which can worsen with extended treatment time. To evaluate DB-020's effectiveness, Decibel Therapeutics designed a double-blind, placebo-controlled Phase 1b clinical trial in which DB-020 was delivered to one ear while the placebo was delivered to the other ear.

17. Was the treatment successful?

The study's results were remarkable. As anticipated, 88% of patients who received a placebo treatment experienced significant ototoxic-related hearing loss in one of their ears – a shocking number to those who are unfamiliar with the prevalence of hearing loss in this population. However, 87% of patients who received DB-020 treatment demonstrated partial or complete protection against ototoxicity in the corresponding ear. Given that tens of thousands of patients in the United States receive cisplatin treatment for various types of cancer, this protective agent could play a vital role in preserving their hearing and enhancing their quality of life after cancer treatment.

18. That’s very promising, indeed. How would my patients find these studies, if they are interested in participating in a clinical trial?

Great question – every clinical trial in the United States is required to register with the website https://clinicaltrials.gov/. This website also hosts trials from around the world. Patients who are interested in participating in different clinical studies should search the database regularly for studies that are listed as “recruiting” for the condition of “sensorineural hearing loss”. After perusing the list of available studies, patients can review the details around the requirements for each study, then reach out to the study team for those that seem interesting to them. Although there aren’t any studies listed for regenerative therapies today (April 2023), we hope there will be more listed in the years to come.

19. Given all of this, if a patient asks me whether they should wait for regenerative technologies before getting a cochlear implant, what should I tell them?

"It's complicated" would likely be the best answer at this point! While it's a personal decision, it's important to consider not only the impact of auditory deprivation on daily life but also the potential for further neural degeneration, particularly in light of future regenerative technologies. Today’s outcomes from cochlear implantation are better understood than tomorrow’s outcomes from regenerative technologies – if there is not sufficient benefit from current technologies, time may be of the essence for your patient to move forward with a cochlear implant. It’s also likely that the first patients to undergo regenerative therapy will have the most limited outcomes, similar to the first patients who received cochlear implants.

Aside from the functional abilities of your patient, it’s important to consider the neural degeneration that can occur without appropriate intervention. Because there is currently no public “launch date” for regenerative technologies, it is likely that patients will need to wait years before regenerative therapies are made available to them.

Although research is being conducted to extend the retracted spiral ganglion neurons to reach the appropriate positions in the inner ear (Schmidbauer recently published in this area), it's in the patient's best interest to proceed with clinical care using the tools available today, such as cochlear implants, for those who are candidates. When regenerative therapies become available, healthcare professionals will be made aware and patients will have more options. It's important to note that regenerative technologies will continue to improve over time, and while the first patients may only achieve partial restoration of hearing, later generations of patients may benefit from more advanced therapies that aim for full restoration of hearing.

20. Sound advice, thank you.

It’s an exciting time in the space of auditory biotechnologies, and I look forward to providing updates in the future!

References

Bermingham, N. A., Hassan, B. A., Wang, V. Y., Fernandez, M., Banfi, S., Bellen, H. J., Fritzsch, B., & Zoghbi, H. Y. (2001). Proprioceptor pathway development is dependent on Math1. Neuron, 30(2), 411–422. https://doi.org/10.1016/s0896-6273(01)00305-1

Chou, C. W., & Hsu, Y. C. (2023). Current development of patient-specific induced pluripotent stem cells harbouring mitochondrial gene mutations and their applications in the treatment of sensorineural hearing loss. Hearing research, 429, 108689. https://doi.org/10.1016/j.heares.2023.108689

Fettiplace, R. (2017). Hair cell transduction, tuning, and synaptic transmission in the mammalian cochlea. Comprehensive Physiology, 7(4), 1197–1227. https://doi.org/10.1002/cphy.c160049

Goudey, B., Plant, K., Kiral, I., Jimeno-Yepes, A., Swan, A., Gambhir, M., Büchner, A., Kludt, E., Eikelboom, R. H., Sucher, C., Gifford, R. H., Rottier, R., & Anjomshoa, H. (2021). A multicenter analysis of factors associated with hearing outcome for 2,735 adults with cochlear implants. Trends in Hearing, 25, 23312165211037525. https://doi.org/10.1177/23312165211037525

Heuermann, M. L., Matos, S., Hamilton, D., & Cox, B. C. (2022). Regenerated hair cells in the neonatal cochlea are innervated and the majority co-express markers of both inner and outer hair cells. Frontiers in Cellular Neuroscience, 16, 841864. https://doi.org/10.3389/fncel.2022.841864

Mainland, J. D., Barlow, L. A., Munger, S. D., Millar, S. E., Vergara, M. N., Jiang, P., Schwob, J. E., Goldstein, B. J., Boye, S. E., Martens, J. R., Leopold, D. A., Bartoshuk, L. M., Doty, R. L., Hummel, T., Pinto, J. M., Trimmer, C., Kelly, C., Pribitkin, E. A., & Reed, D. R. (2020). Identifying treatments for taste and smell disorders: Gaps and opportunities. Chemical Senses, 45(7), 493–502. https://doi.org/10.1093/chemse/bjaa038

Mittal, R., Bencie, N., Langlie, J., Mittal, J., & Eshraghi, A. A. (2021). Exosomes as drug delivery vehicles and biomarkers for neurological and auditory systems. Journal of Cellular Physiology, 236(12), 8035–8049. https://doi.org/10.1002/jcp.30484

Oesterle, E. C., Chien, W. M., & Campbell, S. (2020). Regenerating hair cells: Making sense of all the noise. Neuron, 108(1), 22-34. https://doi.org/10.1016/j.neuron.2020.08.032

Quan, Y. Z., Wei, W., Ergin, V., Rameshbabu, A. P., Huang, M., Tian, C., Saladi, S. V., Indzhykulian, A. A., & Chen, Z. Y. (2023). Reprogramming by drug-like molecules leads to regeneration of cochlear hair cell-like cells in adult mice. Proceedings of the National Academy of Sciences of the United States of America, 120(17), e2215253120. https://doi.org/10.1073/pnas.2215253120

Schmidbauer, D., Fink, S., Rousset, F., Löwenheim, H., Senn, P., & Glueckert, R. (2023). Closing the gap between the auditory nerve and cochlear implant electrodes: Which neurotrophin cocktail performs best for axonal outgrowth and is electrical stimulation beneficial? International Journal of Molecular Sciences, 24(3), 2013. https://doi.org/10.3390/ijms24032013

Shibata, S. B., West, M. B., Du, X., Iwasa, Y., Raphael, Y., & Kopke, R. D. (2020). Gene therapy for hair cell regeneration: Review and new data. Hearing Research, 394, 107981. https://doi.org/10.1016/j.heares.2020.107981

Wan, G., Corfas, G., & Stone, J. S. (2021). Restoration of synapses between hair cells and auditory neurons after noise-induced synaptopathy. eLife, 10, e64760. https://doi.org/10.7554/eLife.64760

Wolff, H., Quigley, T., Raines, S., Oseni, H., Soglia, J., Keilty, J., Qi-Ying, H., Shi, F., Arsenault, B., Whitton, J., & Lee, J. (2023). Development of DB-020, a locally administered product for protection against cisplatin-induced ototoxicity. Paper presented at the Association for Research in Otolaryngology MidWinter Meeting, February 11-15, 2023.

Zheng, J. L., & Gao, W. Q. (2000). Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nature Neuroscience, 3(6), 580–586. https://doi.org/10.1038/75753

Citation 

Lewis, R. M. (2023). 20Q: Auditory biotechnologies - finding their way to the clinic. AudiologyOnline, Article 28618. Available at www.audiologyonline.com

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rebecca m lewis

Rebecca M. Lewis, AuD, PhD

Dr. Rebecca M. Lewis, AuD, PhD, CCC-A, ABAC, is a passionate audiologist and scientist who serves as the Chief of Audiology for the University of California, San Francisco (UCSF), where she directs a collaborative clinical research program and is actively practicing as an audiologist. Dr. Lewis completed her dual doctorates (AuD/PhD) at the University of Washington and trained at other institutions renowned for audiology and hearing science including Massachusetts Eye and Ear and Walter Reed National Military Medical Center before directing a clinical research program at Whisper.ai, a startup hearing aid manufacturer. She is committed to serving her community and the audiology profession, volunteering in other leadership roles including the American Academy of Audiology, the American Tinnitus Association, and the Association for Research in Otolaryngology.



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