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Journal of the Association for Research in Otolaryngology

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Open Access 05-07-2023 | Original Article: General Research

Quantitative Evaluation of the 3D Anatomy of the Human Osseous Spiral Lamina Using MicroCT

Authors: Gabriela O. Bom Braga, Annapaola Parrilli, Robert Zboray, Milica Bulatović, Franca Wagner

Published in: Journal of the Association for Research in Otolaryngology | Issue 4/2023

Abstract

Purpose

The osseous spiral lamina (OSL) is an inner cochlear bony structure that projects from the modiolus from base to apex, separating the cochlear canal into the scala vestibuli and scala tympani. The porosity of the OSL has recently attracted the attention of scientists due to its potential impact on the overall sound transduction. The bony pillars between the vestibular and tympanic plates of the OSL are not always visible in conventional histopathological studies, so imaging of such structures is usually lacking or incomplete. With this pilot study, we aimed, for the first time, to anatomically demonstrate the OSL in great detail and in 3D.

Methods

We measured width, thickness, and porosity of the human OSL by microCT using increasing nominal resolutions up to 2.5-µm voxel size. Additionally, 3D models of the individual plates at the basal and middle turns and the apex were created from the CT datasets.

Results

We found a constant presence of porosity in both tympanic plate and vestibular plate from basal turn to the apex. The tympanic plate appears to be more porous than vestibular plate in the basal and middle turns, while it is less porous in the apex. Furthermore, the 3D reconstruction allowed the bony pillars that lie between the OSL plates to be observed in great detail.

Conclusion

By enhancing our comprehension of the OSL, we can advance our comprehension of hearing mechanisms and enhance the accuracy and effectiveness of cochlear models.

Corti A (1851) Recherches sur l’organe de L’ouie des Mamiferes. Akademische Verlagsgesellschaft, Z. Wiss Zool

Neubert K (1950) Die Basilarmembran Des Menschen Und Ihr Verankerungssystem. Z Anat Entwicklungsgesch 114:540–590

Lim D (1970) Surface ultrastructure of the cochlear perilymphatic space. J Laryngol Otol 84(4):413–428. https://doi.org/10.1017/s0022215100072029CrossRefPubMed

Shepherd RK, Colreavy MP (2004) Surface microstructure of the perilymphatic space: implications for cochlear implants and cell- or drug-based therapies. Arch Otolaryngol Head Neck Surg 130(5):518–523. https://doi.org/10.1001/archotol.130.5.518CrossRefPubMed

Raufer S, Guinan JJ Jr, Nakajima HH (2019) Cochlear partition anatomy and motion in humans differ from the classic view of mammals. Proc Natl Acad Sci USA 116(28):13977–13982. https://doi.org/10.1073/pnas.1900787116CrossRefPubMedPubMedCentral

Raufer S, Idoff C, Zosuls A, Marino G, Blanke N, Bigio IJ, O’Malley JT, Burgess BJ, Nadol JB, Guinan JJ Jr, Nakajima HH (2020) Anatomy of the human osseous spiral lamina and cochlear partition bridge: relevance for cochlear partition motion. J Assoc Res Otolaryngol 21(2):171–182. https://doi.org/10.1007/s10162-020-00748-1CrossRefPubMedPubMedCentral

Stenfelt S, Puria S, Hato N, Goode RL (2003) Basilar membrane and osseous spiral lamina motion in human cadavers with air and bone conduction stimuli. Hear Res 181(1–2):131–143. https://doi.org/10.1016/s0378-5955(03)00183-7CrossRefPubMed

Cunha L, Horvath I, Ferreira S, Lemos J, Costa P, Vieira D, Veres DS, Szigeti K, Summavielle T, Mathe D, Metello LF (2014) Preclinical imaging: an essential ally in modern biosciences. Mol Diagn Ther 18(2):153–173. https://doi.org/10.1007/s40291-013-0062-3CrossRefPubMed

Woods A, Ellis R (eds.) (1994) Laboratory histopathology: a complete reference. New York: Churchill Livingstone. Vol. 7:2-10

10.

Iyer JS, Zhu N, Gasilov S, Ladak HM, Agrawal SK, Stankovic KM (2018) Visualizing the 3D cytoarchitecture of the human cochlea in an intact temporal bone using synchrotron radiation phase contrast imaging. Biomed Opt Express 9(8):3757–3767. https://doi.org/10.1364/BOE.9.003757CrossRefPubMedPubMedCentral

11.

Bom Braga GO, Schneider D, Weber S, Caversaccio M (2021) Computer assistance, image guidance and robotics in otologic surgery. In Bento RF, Lima Júnior LRP,Tsuji RK, Goffi-Gomez MVS, Lima DdVSP, Brito Rd (eds.) Tratado de Implante Coclear e Próteses Auditivas Implantáveis. Thieme Revinter: Rio de Janeiro, Brazil

12.

Bellos C, Rigas G, Spiridon IF, Bibas A, Iliopoulou D, Böhnke F, Koutsouris D, Fotiadis DI (2014) Reconstruction of cochlea based on micro-CT and histological images of the human inner ear. BioMed Res Int 2014:485783. https://doi.org/10.1155/2014/485783

13.

Rau TS, Rau TS, Würfel W, Lenarz T, Majdani O et al (2013) Three-dimensional histological specimen preparation for accurate imaging and spatial reconstruction of the middle and inner ear. Int J Comput Assisted Radiol Surg 8(4):481–509. https://doi.org/10.1007/s11548-013-0825-7CrossRef

14.

Walton LA, Bradley RS, Withers PJ, Newton VL, Watson REB, Austin C, Sherratt MJ (2015) Morphological characterisation of unstained and intact tissue micro-architecture by X-ray computed micro- and nano-tomography. Sci Rep 5. https://doi.org/10.1038/srep10074

15.

Küçük B, Abe K, Ushiki T, Inuyama Y, Fukuda S, Ishikavva K (1991) Microstructures of the bony modiolus in the human cochlea: a scanning electron microscopic study. Microsc 40(3):193–197. https://doi.org/10.1093/oxfordjournals.jmicro.a050895CrossRef

16.

Fleischer G (1973) Studien Am Skelett Des Gehoerhörgans Der Säugetriere Einschließlich Des Menschen. Säugetrierkundliche Mitteilungen 2(3):131–239

17.

Homer M, Champneys A, Hunt G, Cooper N (2004) Mathematical modeling of the radial profile of basilar membrane vibrations in the inner ear. J Acoust Soc Am 116(2):1025–1034. https://doi.org/10.1121/1.1771571CrossRefPubMed

18.

Tonndorf J (1966). Bone conduction. Studies in experimental animals. Acta Otolaryngol:Suppl 213:1+

19.

Stenfelt S (2015) Inner ear contribution to bone conduction hearing in the human. Hear Res 329:41–51. https://doi.org/10.1016/j.heares.2014.12.003

20.

Stenfelt S (2020) Investigation of mechanisms in bone conduction hyperacusis with third window pathologies based on model predictions. Front Neurol 11:966. https://doi.org/10.3389/fneur.2020.00966

21.

Gulya AJ, Minor LB, Poe DS (2010) Glasscock-Shambaugh surgery of the ear. 6 edn., pp 643–79

22.

O'Toole Bom Braga G, Zboray R, Parrilli A, Bulatovic M, Caversaccio MD, Wagner F (2022) Otosclerosis under microCT: new insights into the disease and its anatomy. Front Radiol 2. https://doi.org/10.3389/fradi.2022.965474

23.

Navarro M, Ruberte J, Carretero A (2017) 15 - Vestibulocochlear organ. In Ruberte J, Carretero A, Navarro M (eds.) Morphological Mouse Phenotyping: Anatomy, Histology and Imaging, pp. 521-539. https://doi.org/10.1016/B978-0-12-812972-2.50015-5

24.

Forge A, Wright T (2002) The molecular architecture of the inner ear. Br Med Bull 63:5–24. https://doi.org/10.1093/bmb/63.1.5CrossRefPubMed

25.

Küçük B, Abe K, Ushiki T, Inuyama Y, Fukuda S, Ishikawa K (1991) Microstructures of the bony modiolus in the human cochlea : a scanning electron microscopic study. J Electron Microsc 40(40):193–197

26.

Matenaers C, Popper B, Rieger A, Wanke R, Blutke A (2018). Practicable methods for histological section thickness measurement in quantitative stereological analyses. PLoS One 13(2):e0192879. https://doi.org/10.1371/journal.pone.0192879

27.

Brunschwig AS, Salt AN (1997) Fixation-induced shrinkage of Reissner’s membrane and its potential influence on the assessment of endolymph volume. Hear Res 114(1–2):62–68. https://doi.org/10.1016/s0378-5955(97)00153-6CrossRefPubMed

28.

Kampschulte M, Langheinirch AC, Sender J, Litzlbauer HD, Althohn U, Schwab JD, Alejandre-Lafont E, Martels G, Krombach GA (2016) Nano-computed tomography: technique and applications. Rofo 188(2):146–154. https://doi.org/10.1055/s-0041-106541CrossRefPubMed

29.

Bayraktar HH, Morgan EF, Niebur GL, Morris GE, Wong EK, Keaveny TM (2004) Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J Biomech 37(1):27–35. https://doi.org/10.1016/S0021-9290(03)00257-4CrossRefPubMed

30.

Sellon JB, Ghaffari R, Farrahi S, Richardson GP, Freeman DM (2014) Porosity controls spread of excitation in tectorial membrane traveling waves. Biophys J 106(6):1406–1413. https://doi.org/10.1016/j.bpj.2014.02.012CrossRefPubMedPubMedCentral

31.

Hahn H, Salt AN, Biegner T, Kammerer B, Delabar U, Hartsock JJ, Plontke SK (2012) Dexamethasone levels and base-to-apex concentration gradients in the scala tympani perilymph after intracochlear delivery in the guinea pig. Otol Neurotol 33(4):660–665. https://doi.org/10.1097/MAO.0b013e318254501bCrossRefPubMedPubMedCentral

32.

Hahn H, Salt AN, Schumacher U, Plontke SK (2013) Gentamicin concentration gradients in scala tympani perilymph following systemic applications. Audiol Neurootol 18(6):383–391. https://doi.org/10.1159/000355283CrossRefPubMed

33.

Plontke SK, Biegner T, Kammerer B, Delabar U, Salt AN (2008) Dexamethasone concentration gradients along scala tympani after application to the round window membrane. Otol Neurotol 29(3):401–406. https://doi.org/10.1097/MAO.0b013e318161aaaeCrossRefPubMed

34.

Plontke SK, Wood AW, Salt AN (2002) Analysis of gentamicin kinetics in fluids of the inner ear with round window administration. Otol Neurotol 23(6):967–974. https://doi.org/10.1097/00129492-200211000-00026CrossRefPubMed

35.

Salt AN, Hartsock JJ, Gill RM, Piu F, Plontke SK (2012) Perilymph pharmacokinetics of markers and dexamethasone applied and sampled at the lateral semi-circular canal. J Assoc Res Otolaryngol 13(6):771–783. https://doi.org/10.1007/s10162-012-0347-yCrossRefPubMedPubMedCentral

36.

Salt AN, Hale SA, Plonkte SK (2006) Perilymph sampling from the cochlear apex: a reliable method to obtain higher purity perilymph samples from scala tympani. J Neurosci Methods 153(1):121–129. https://doi.org/10.1016/j.jneumeth.2005.10.008CrossRefPubMed

37.

Salt AN, Hirose K (2018) Communication pathways to and from the inner ear and their contributions to drug delivery. Hear Res 362:25–37. https://doi.org/10.1016/j.heares.2017.12.010CrossRefPubMed

38.

Li D, Sun J, Zhao L, Guo W, Sun W, Yang S (2017) Aminoglycoside increases permeability of osseous spiral laminae of cochlea by interrupting MMP-2 and MMP-9 balance. Neurotox Res 31(3):348–357. https://doi.org/10.1007/s12640-016-9689-2CrossRefPubMed

39.

Atkinson PJ, Wise AK, Flynn BO, Nayagam BA, Hume CR, O'Leary SJ, Shepherd RK, Richardson RT (2012). Neurotrophin gene therapy for sustained neural preservation after deafness. PLoS One 7(12):e52338. https://doi.org/10.1371/journal.pone.0052338

40.

Tan J, Wang Y, Yip X, Glynn F, Shepherd RK, Caruso F (2012) Nanoporous peptide particles for encapsulating and releasing neurotrophic factors in an animal model of neurodegeneration. Adv Mater 24(25):3362–3366. https://doi.org/10.1002/adma.201200634CrossRefPubMedPubMedCentral

41.

van Loon MC, Ramekers D, Agterberg MJ, de Groot JC, Grolman W, Klis SF, Versnel H (2013) Spiral ganglion cell morphology in guinea pigs after deafening and neurotrophic treatment. Hear Res 298:17–26. https://doi.org/10.1016/j.heares.2013.01.013CrossRefPubMed

42.

Zhang YZW, Johnston AH, Newman TA, Pyykk I, Zou J (2011) Comparison of the distribution pattern of PEG-b-PCL polymersomes delivered into the rat inner ear via different methods. Acta Otolaryngol 131:1249–1256. https://doi.org/10.3109/00016489.2011.615066CrossRefPubMed

43.

Plontke SK, Mynatt R, Gill RM, Borgmann S, Salt AN (2007) Concentration gradient along the scala tympani after local application of gentamicin to the round window membrane. Laryngoscope 117(7):1191–1198. https://doi.org/10.1097/MLG.0b013e318058a06bCrossRefPubMedPubMedCentral

44.

Ciuman RR (2009) Communication routes between intracranial spaces and inner ear: function, pathophysiologic importance and relations with inner ear diseases. Am J Otolaryngol 30(3):193–202. https://doi.org/10.1016/j.amjoto.2008.04.005CrossRefPubMed

45.

Bielefeld EC, Kobel MJ (2019) Advances and challenges in pharmaceutical therapies to prevent and repair cochlear injuries from noise. Front Cell Neurosci 13:285. https://doi.org/10.3389/fncel.2019.00285CrossRefPubMedPubMedCentral

Title: Quantitative Evaluation of the 3D Anatomy of the Human Osseous Spiral Lamina Using MicroCT
Authors: Gabriela O. Bom Braga
Annapaola Parrilli
Robert Zboray
Milica Bulatović
Franca Wagner
Publication date: 05-07-2023
Publisher: Springer US
Published in: Journal of the Association for Research in Otolaryngology / Issue 4/2023
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-023-00904-3

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Quantitative Evaluation of the 3D Anatomy of the Human Osseous Spiral Lamina Using MicroCT

Abstract

Purpose

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

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