Anatomic, physiologic, and proteomic consequences of repeated microneedle-mediated perforations of the round window membrane.


Journal

Hearing research
ISSN: 1878-5891
Titre abrégé: Hear Res
Pays: Netherlands
ID NLM: 7900445

Informations de publication

Date de publication:
05 2023
Historique:
received: 25 09 2022
revised: 20 02 2023
accepted: 12 03 2023
medline: 28 4 2023
pubmed: 27 3 2023
entrez: 26 3 2023
Statut: ppublish

Résumé

We have developed 3D-printed microneedle technology for diagnostic aspiration of perilymph and intracochlear delivery of therapeutic agents. Single microneedle-mediated round window membrane (RWM) perforation does not cause hearing loss, heals within 48-72 h, and yields sufficient perilymph for proteomic analysis. In this study, we investigate the anatomic, physiologic, and proteomic consequences of repeated microneedle-mediated perforations of the same RWM at different timepoints. 100-μm-diameter hollow microneedles were fabricated using two-photon polymerization (2PP) lithography. The tympanic bullae of Hartley guinea pigs (n = 8) were opened with adequate exposure of the RWM. Distortion product otoacoustic emissions (DPOAE) and compound action potential (CAP) were recorded to assess hearing. The hollow microneedle was introduced into the bulla and the RWM was perforated; 1 μL of perilymph was aspirated from the cochlea over the course of 45 s. 72 h later, the above procedure was repeated with aspiration of an additional 1 μL of perilymph. 72 h after the second perforation, RWMs were harvested for confocal imaging. Perilymph proteomic analysis was completed using liquid chromatography-tandem mass spectrometry (LC-MS/MS). Two perforations and aspirations were performed in 8 guinea pigs. In six, CAP, DPOAE, and proteomic analysis were obtained; in one, only CAP and DPOAE results were obtained; and in one, only proteomics results were obtained. Hearing tests demonstrated mild hearing loss at 1-4 kHz and 28 kHz, most consistent with conductive hearing loss. Confocal microscopy demonstrated complete healing of all perforations with full reconstitution of the RWM. Perilymph proteomic analysis identified 1855 proteins across 14 samples. The inner ear protein cochlin was observed in all samples, indicating successful aspiration of perilymph. Non-adjusted paired t-tests with p < 0.01 revealed significant changes in 13 of 1855 identified proteins (0.7%) between the first and second aspirations. We demonstrate that repeated microneedle perforation of the RWM is feasible, allows for complete healing of the RWM, and minimally changes the proteomic expression profile. Thus, microneedle-mediated repeated aspirations in a single animal can be used to monitor the response to inner ear treatments over time.

Sections du résumé

BACKGROUND
We have developed 3D-printed microneedle technology for diagnostic aspiration of perilymph and intracochlear delivery of therapeutic agents. Single microneedle-mediated round window membrane (RWM) perforation does not cause hearing loss, heals within 48-72 h, and yields sufficient perilymph for proteomic analysis. In this study, we investigate the anatomic, physiologic, and proteomic consequences of repeated microneedle-mediated perforations of the same RWM at different timepoints.
METHODS
100-μm-diameter hollow microneedles were fabricated using two-photon polymerization (2PP) lithography. The tympanic bullae of Hartley guinea pigs (n = 8) were opened with adequate exposure of the RWM. Distortion product otoacoustic emissions (DPOAE) and compound action potential (CAP) were recorded to assess hearing. The hollow microneedle was introduced into the bulla and the RWM was perforated; 1 μL of perilymph was aspirated from the cochlea over the course of 45 s. 72 h later, the above procedure was repeated with aspiration of an additional 1 μL of perilymph. 72 h after the second perforation, RWMs were harvested for confocal imaging. Perilymph proteomic analysis was completed using liquid chromatography-tandem mass spectrometry (LC-MS/MS).
RESULTS
Two perforations and aspirations were performed in 8 guinea pigs. In six, CAP, DPOAE, and proteomic analysis were obtained; in one, only CAP and DPOAE results were obtained; and in one, only proteomics results were obtained. Hearing tests demonstrated mild hearing loss at 1-4 kHz and 28 kHz, most consistent with conductive hearing loss. Confocal microscopy demonstrated complete healing of all perforations with full reconstitution of the RWM. Perilymph proteomic analysis identified 1855 proteins across 14 samples. The inner ear protein cochlin was observed in all samples, indicating successful aspiration of perilymph. Non-adjusted paired t-tests with p < 0.01 revealed significant changes in 13 of 1855 identified proteins (0.7%) between the first and second aspirations.
CONCLUSIONS
We demonstrate that repeated microneedle perforation of the RWM is feasible, allows for complete healing of the RWM, and minimally changes the proteomic expression profile. Thus, microneedle-mediated repeated aspirations in a single animal can be used to monitor the response to inner ear treatments over time.

Identifiants

pubmed: 36966687
pii: S0378-5955(23)00051-5
doi: 10.1016/j.heares.2023.108739
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

108739

Subventions

Organisme : NIDCD NIH HHS
ID : R01 DC014547
Pays : United States

Informations de copyright

Copyright © 2023. Published by Elsevier B.V.

Auteurs

Stephen Leong (S)

Vagelos College of Physicians & Surgeons, Columbia University Irving Medical Center, New York, NY, United States.

Aykut Aksit (A)

Department of Mechanical Engineering, Columbia University, New York, NY, United States.

Betsy Szeto (B)

Vagelos College of Physicians & Surgeons, Columbia University Irving Medical Center, New York, NY, United States; Department of Otolaryngology - Head & Neck Surgery, University of Virginia Health System, Charlottesville, VA.

Sharon J Feng (SJ)

Vagelos College of Physicians & Surgeons, Columbia University Irving Medical Center, New York, NY, United States.

Xiang Ji (X)

Department of Chemistry, Barnard College, New York, NY, United States.

Rajesh K Soni (RK)

Proteomics and Macromolecular Crystallography Core, Columbia University Irving Medical Center, New York, NY, United States.

Elizabeth S Olson (ES)

Department of Otolaryngology - Head & Neck Surgery, New-York Presbyterian / Columbia University Irving Medical Center, New York, NY, United States.

Jeffrey W Kysar (JW)

Department of Mechanical Engineering, Columbia University, New York, NY, United States; Department of Otolaryngology - Head & Neck Surgery, New-York Presbyterian / Columbia University Irving Medical Center, New York, NY, United States.

Anil K Lalwani (AK)

Vagelos College of Physicians & Surgeons, Columbia University Irving Medical Center, New York, NY, United States; Department of Mechanical Engineering, Columbia University, New York, NY, United States; Department of Otolaryngology - Head & Neck Surgery, New-York Presbyterian / Columbia University Irving Medical Center, New York, NY, United States. Electronic address: akl2144@cumc.columbia.edu.

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