Visualization of ex vivo rabbit olfactory mucosa and foramina with three-dimensional optical coherence tomography.

Anterior skull base Cribriform plate Olfactory cleft Olfactory foramina Olfactory mucosa Optical coherence tomography

Journal

Lasers in medical science
ISSN: 1435-604X
Titre abrégé: Lasers Med Sci
Pays: England
ID NLM: 8611515

Informations de publication

Date de publication:
Oct 2022
Historique:
received: 23 10 2021
accepted: 19 06 2022
pubmed: 3 7 2022
medline: 5 10 2022
entrez: 2 7 2022
Statut: ppublish

Résumé

There is increasing interest in developing a minimally invasive imaging modality to safely evaluate dynamic microscopic changes of the olfactory mucosa and cribriform foramina. Herein, we utilized three-dimensional (3D) optical coherence tomography (OCT) to characterize the ex vivo stratified substructure of olfactory mucosa in rabbits and create 3D reconstructed images of olfactory foramina. Olfactory mucosa and cribriform plates from four New Zealand White rabbits were dissected and imaged using two swept-source OCT systems: (1) 1.3-µm (μm) center wavelength, 100-nm bandwidth, 200-kHz sweep rate, and (2) 1.7-μm center wavelength, 120-nm bandwidth, 90-kHz sweep rate. Volumetric OCT images were compiled to create a 3D reconstruction of the cribriform plate. The ability of OCT to distinguish the olfactory mucosa substructure and foramina was compared to histology. To estimate imaging penetration depth of each system, the first-order exponential decays of depth-resolved intensity were calculated and compared using a paired t-test. Three-dimensional OCT depicted the stratified layered structures within the olfactory mucosa correlating with histology. The epithelium and lamina propria were measured to be 32 μm and 107 μm in 1.3-μm OCT compared to 30 μm and 105 μm in histology. Olfactory foramina were visualized via 3D reconstruction. The 1.7-μm system provided greater depth penetration compared to the 1.3-μm system, allowing for improved foramina visualization. We have shown that OCT can be used to image non-pathologic olfactory mucosa and foramina. Implications for this work include diagnostic and therapeutic potentials for neurorhinological and neurodegenerative diseases.

Identifiants

pubmed: 35779115
doi: 10.1007/s10103-022-03598-w
pii: 10.1007/s10103-022-03598-w
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3203-3211

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer-Verlag London Ltd., part of Springer Nature.

Références

Godoy MDCL, Voegels RL, Pinna FDR, Imamura R, Farfel JM (2015) Olfaction in neurologic and neurodegenerative diseases: a literature review. Int Arch Otorhinolaryngol 19:176–179
pubmed: 25992176
Lanza DC, Moran DT, Doty RL, Trojanowski JQ, Lee JH, Rowley JC, Crawford D, Kennedy DW (1993) Endoscopic human olfactory biopsy technique. Laryngoscope 103:815–819
pubmed: 8341109
Doty RL (2009) The olfactory system and its disorders. Semin Neurol 29:74–81
pubmed: 19214935
Joseph T, Auger SD, Peress L, Rack D, Cuzick J, Giovannoni G, Lees A, Schrag AE, Noyce AJ (2019) Screening performance of abbreviated versions of the UPSIT smell test. J Neurol 266:1897–1906
pubmed: 31053960 pmcid: 6647236
Doty RL (2012) Olfaction in Parkinson’s disease and related disorders. Neurobiol Dis 46:527–552
pubmed: 22192366
Ross GW, Petrovitch H, Abbott RD, Tanner CM, Popper J, Masaki K, Launer L, White LR (2008) Association of olfactory dysfunction with risk for future Parkinson’s disease. Ann Neurol 63:167–173
pubmed: 18067173
Zou YM, Lu D, Liu LP, Zhang HH, Zhou YY (2016) Olfactory dysfunction in Alzheimer’s disease. Neuropsychiatr Dis Treat 12:869–875
pubmed: 27143888 pmcid: 4841431
Lee JH, Goedert M, Hill WD, Lee VM, Trojanowski JQ (1993) Tau proteins are abnormally expressed in olfactory epithelium of Alzheimer patients and developmentally regulated in human fetal spinal cord. Exp Neurol 121:93–105
pubmed: 8495714
Trojanowski JQ, Newman PD, Hill WD, Lee VM (1991) Human olfactory epithelium in normal aging, Alzheimer’s disease, and other neurodegenerative disorders. J Comp Neurol 310:365–376
pubmed: 1723988
Crino PB, Greenberg B, Martin JA, Lee VM, Hill WD, Trojanowski JQ (1995) β-amyloid peptide and amyloid precursor proteins in olfactory mucosa of patients with Alzheimer’s disease, Parkinson’s disease, and Down syndrome. Ann Otol Rhinol Laryngol 104:655–661
pubmed: 7639477
Holbrook EH, Leopold DA, Schwob JE (2005) Abnormalities of axon growth in human olfactory mucosa. Laryngoscope 115:2144–2154
pubmed: 16369158
Paik SI, Lehman MN, Seiden AM, Duncan HJ, Smith DV (1992) Human olfactory biopsy: the influence of age and receptor distribution. Arch Otolaryngol Neck Surg 118:731–738
Lane AP, Gomez G, Dankulich T, Wang H, Bolger WE, Rawson NE (2002) The superior turbinate as a source of functional human olfactory receptor neurons. Laryngoscope 112:1183–1189
pubmed: 12169895
Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W, Hee MR, Flotte T, Gregory K, Puliafito CA, Fujimoto JG (1991) Optical coherence tomography. Science 254:11783–21181
Chiu SC, Hung HS, Lin SZ, Chiang E, Liu DD (2009) Therapeutic potential of olfactory ensheathing cells in neurodegenerative diseases. J Mol Med 87:1179–1189
pubmed: 19756447
Mackay-Sim A, Féron F, Cochrane J, Bassingthwaighte L, Bayliss C, Davies W, Fronek P, Gray C, Kerr G, Licina P, Nowitzke A, Perry C, Silburn PAS, Urquhart S, Geraghty T (2008) Autologous olfactory ensheathing cell transplantation in human paraplegia: A 3-year clinical trial. Brain 131:2376–2386
pubmed: 18689435 pmcid: 2525447
Lima C, Pratas-Vital J, Escada P, Hasse-Ferreira A, Capucho C, Peduzzi JD (2006) Olfactory mucosa autografts in human spinal cord injury: a pilot clinical study. J Spinal Cord Med 29:191–203
pubmed: 16859223 pmcid: 1864811
Murrell W, Wetzig A, Donnellan M, Féron F, Burne T, Meedeniya A, Kesby J, Bianco J, Perry C, Silburn P, Mackay-Sim A (2008) Olfactory mucosa is a potential source for autologous stem cell therapy for Parkinson’s disease. Stem Cells 26:2183–2192
pubmed: 18535154
Pereira ME, Macri NP, Creasy DM (2011) Evaluation of the rabbit nasal cavity in inhalation studies and a comparison with other common laboratory species and man. Toxicol Pathol 39:893–900
pubmed: 21628717
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682
pubmed: 22743772
Rolls G (2011) Difficult blocks and reprocessing. Leica Microsyst 9:1–108
Camacho S, Ostos-Garrido MV, Domezain A, Carmona R (2010) Study of the olfactory epithelium in the developing sturgeon. Characterization of the crypt cells. Chem Senses 35:147–156
pubmed: 20032110
De Rezende PF, Ctenas B, Weber R, Saldiva PH, Voegels RL (2013) Olfactory neuroepithelium in the superior and middle turbinates: which is the optimal biopsy site? Int Arch Otorhinolaryngol 17:131–138
Graziadei PP, Graziadei GA (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1–18
pubmed: 438867
Boesveldt S, Postma EM, Boak D, Welge-Luessen A, Schöpf V, Mainland JD, Martens J, Ngai J, Duffy VB (2017) Anosmia-A clinical review. Chem Senses 42:513–523
pubmed: 28531300 pmcid: 5863566
Edge AS, Chen ZY (2008) Hair cell regeneration. Curr Opin Neurobiol 18:377–382
pubmed: 18929656 pmcid: 5653255
Drexler W, Fujimoto JG (2015) Optical coherence tomography: technology and applications, 2nd edn. Switzerland
Krauss JM, Puliafito CA (1995) Lasers in ophthalmology. Lasers Surg Med 17:102–159
pubmed: 8569410
Welzel J (2001) Optical coherence tomography in dermatology: a review. Ski Res Technol 7:1–9
Mahmood U, Ridgway J, Jackson R, Guo S, Su J, Armstrong W, Shibuya T, Crumley R, Chen Z, Wong B (2006) In vivo optical coherence tomography of the nasal mucosa. Am J Rhinol 20:155–159
pubmed: 16686378
Ueda T, Sakamoto T, Kobayashi M, Kuwata F, Ishikawa M, Omori K, Nakagawa T (2019) Optical coherence tomography for observation of the olfactory epithelium in mice. Auris Nasus Larynx 46:230–237
pubmed: 30170907
Girerd C, Lihoreau T, Rabenorosoa K, Tamadazte B, Benassarou M, Tavernier L, Pazart L, Haffen E, Andreff N, Renaud P (2018) In vivo inspection of the olfactory epithelium: feasibility of robotized optical biopsy. Ann Biomed Eng 46:1951–1961
pubmed: 29922959
Farneti P, Riboldi A, Sciarretta V, Piccin O, Tarchini P, Pasquini E (2017) Usefulness of three-dimensional computed tomographic anatomy in endoscopic frontal recess surgery. Surg Radiol Anat 39:161–168
pubmed: 27192983
Bird DJ, Amirkhanian A, Pang B, Van Valkenburgh B (2014) Quantifying the cribriform plate: influences of allometry, function, and phylogeny in carnivora. Anat Rec 297:2080–2092
Miyake MM, Bleier BS (2015) Bypassing the blood–brian barrier using established skull base reconstruction techniques. World J Otorhinolaryngol Neck Surg 1:11–16
Dhuria SV, Hanson LR, Frey WH (2010) Intranasal delivery to the central nervous system: mechanisms and experimental considerations. J Pharm Sci 99:1654–1673
pubmed: 19877171
Li Y, Jing J, Heidari E, Zhu J, Qu Y, Chen Z (2017) Intravascular optical coherence tomography for characterization of atherosclerosis with a 1.7 micron swept-source laser. Sci Rep 7:14525
Pham TT, Chen L, Heidari AE, Chen JJ, Zhukhovitskaya A, Li Y, Patel U, Chen Z, Wong BJF (2019) Computational analysis of six optical coherence tomography systems for vocal fold imaging: a comparison study. Lasers Surg Med. https://doi.org/10.1001/lsm.23060
Li Y, Sudol NT, Miao Y, Jing JC, Zhu J, Lane F, Chen Z (2019) 1.7 micron optical coherence tomography for vaginal tissue characterization in vivo. Lasers Surg Med 51:120–126
pubmed: 30058722
Lin JL, Yau AY, Boyd J, Hamamoto A, Su E, Tracey L, Heidari AE, Wang AH, Ahuja G, Chen Z, Wong BJ (2013) Real-time subglottic stenosis imaging using optical coherence tomography in the rabbit. JAMA Otolaryngol Head Neck Surg 139:502–509
pubmed: 23681033 pmcid: 3893145
Liu G, Rubinstein M, Saidi A, Qi W, Foulad A, Wong B, Chen Z (2011) Imaging vibrating vocal folds with a high speed 1050 nm swept source OCT and ODT. Opt Express 19:11880–11889
pubmed: 21716421 pmcid: 3130610
Tang S, Jung W, McCormick D, Xie T, Su J, Ahn Y-C, Tromberg BJ, Chen Z (2009) Design and implementation of fiber-based multiphoton endoscopy with microelectromechanical systems scanning. J Biomed Opt 14:034005
pubmed: 19566298
Jung W, Tang S, McCormic DT, Xie T, Ahn Y-C, Su J, Tomov IV, Krasieva TB, Tromberg BJ, Chen Z (2008) Miniaturized probe based on a microelectromechanical system mirror for multiphoton microscopy. Opt Lett 33:1324–1326
pubmed: 18552946 pmcid: 2613774
Miao Y, Brenner M, Chen Z (2019) Endoscopic optical coherence tomography for assessing inhalation airway injury: a technical review. Otolaryngol (Sunnyvale) 9:366

Auteurs

Tiffany Thienthao Pham (TT)

Beckman Laser Institute & Medical Clinic, University of California - Irvine, Irvine, CA, USA.

Andrew Emon Heidari (AE)

Beckman Laser Institute & Medical Clinic, University of California - Irvine, Irvine, CA, USA.
Department of Biomedical Engineering, University of California - Irvine, Irvine, CA, USA.

Amir Aaron Hakimi (AA)

Beckman Laser Institute & Medical Clinic, University of California - Irvine, Irvine, CA, USA.

Yan Li (Y)

Beckman Laser Institute & Medical Clinic, University of California - Irvine, Irvine, CA, USA.
Department of Biomedical Engineering, University of California - Irvine, Irvine, CA, USA.

Cameron Michael Heilbronn (CM)

Beckman Laser Institute & Medical Clinic, University of California - Irvine, Irvine, CA, USA.
Department of Otolaryngology - Head and Neck Surgery, University of California - Irvine, School of Medicine, Orange, CA, USA.

Ellen Minyoung Hong (EM)

Beckman Laser Institute & Medical Clinic, University of California - Irvine, Irvine, CA, USA.

Ji-Hun Mo (JH)

Beckman Laser Institute - Korea, Dankook University, Cheonan, Chungnam, Republic of Korea.
Department of Otorhinolaryngology-Head and Neck Surgery, Dankook University, Cheonan, Chungnam, Republic of Korea.

Edward Cheng-Lung Kuan (EC)

Department of Otolaryngology - Head and Neck Surgery, University of California - Irvine, School of Medicine, Orange, CA, USA.

Zhongping Chen (Z)

Beckman Laser Institute & Medical Clinic, University of California - Irvine, Irvine, CA, USA.
Department of Biomedical Engineering, University of California - Irvine, Irvine, CA, USA.

Brian Jet-Fei Wong (BJ)

Beckman Laser Institute & Medical Clinic, University of California - Irvine, Irvine, CA, USA. bjwong@uci.edu.
Department of Biomedical Engineering, University of California - Irvine, Irvine, CA, USA. bjwong@uci.edu.
Department of Otolaryngology - Head and Neck Surgery, University of California - Irvine, School of Medicine, Orange, CA, USA. bjwong@uci.edu.

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