Evaluation of the Human Vocal Fold Lamina Propria Development Using Optical Coherence Tomography.
Vocal fold
development
extracellular matrix
lamina propria
larynx
optical coherence tomography
optical imaging
pediatric
Journal
The Laryngoscope
ISSN: 1531-4995
Titre abrégé: Laryngoscope
Pays: United States
ID NLM: 8607378
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
revised:
17
02
2021
received:
06
12
2020
accepted:
09
03
2021
pubmed:
19
3
2021
medline:
21
9
2021
entrez:
18
3
2021
Statut:
ppublish
Résumé
Identifying distinctive features of the vocal fold (VF) during development could have significant clinical implications for treating voice disorders. This study investigates the structural organization of the VF microanatomy across gender and age groups using optical coherence tomography (OCT). Prospective clinical trial. In vivo OCT images were acquired from 97 patients (58 males and 39 females) aged between 6 weeks and 27 years. All patients showed no signs of vocal fold pathology on endoscopy. Morphological features were extracted from OCT images and statistically compared between age groups. This study was performed at Massachusetts Eye and Ear between 2017 and 2019. All OCT acquisitions show a stratified microanatomy across age groups, even in newborns suggesting the presence of a superficial lamina propria (SLP) at birth. Furthermore, the optical scattering in the VF lamina propria changes according to age, suggesting subepithelial maturation. Although the epithelium thickness was relatively constant across age groups, the SLP showed a significant linear relationship between age and thickness (P = .016). Furthermore, a significant difference (P = .002) in SLP thickness was found between young adult males and females. The overall thickness of the entire mucosa did not change significantly with age. OCT is a noninvasive imaging modality capable of providing quantitative morphological features to describe the VF development. A stratified structure can be observed in OCT from newborns to young adults. Further investigations could combine OCT, acoustic measurements, and molecular sensitive techniques to provide a complete interpretation of the VF development. NA Laryngoscope, 131:E2558-E2565, 2021.
Types de publication
Clinical Trial
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
E2558-E2565Subventions
Organisme : Massachusetts Eye and Ear Infirmary
Informations de copyright
© 2021 The American Laryngological, Rhinological and Otological Society, Inc.
Références
Sulter AM, Schutte HK, Miller DG. Differences in phonetogram features between male and female subjects with and without vocal training. J Voice 1995;9:363-377.
Traunmüller H, Eriksson A. The frequency range of the voice fundamental in the speech of male and female adults. Dep Linguist Univ Stock 1994;97:1905191-1905195.
Awd Allah RS, Dkhil MA, Farhoud E. Fibroblasts in the human vocal fold mucosa: an ultrastructural study of different age groups. Singapore Med J 2009;50:201-207.
Sato K, Hirano M, Nakashima T. 3D structure of the macula flava in the human vocal fold. Acta Otolaryngol 2003;123:269-273.
Sato K, Umeno H, Nakashima T, Nonaka S, Harabuchi Y. Histopathologic investigations of the unphonated human child vocal fold mucosa. J Voice 2012;26:37-43.
Gray SD, Pignatari SS, Harding P. Morphologic ultrastructure of anchoring fibers in normal vocal fold basement membrane zone. J Voice 1994;8:48-52.
Ishii K, Zhai WG, Akita M, Hirose H. Ultrastructure of the lamina propria of the human vocal fold. Acta Otolaryngol 1996;116:778-782.
Sato K, Hirano M, Nakashima T. Fine structure of the human newborn and infant vocal fold mucosae. Ann Otol Rhinol Laryngol 2001;110:417-424.
De Melo ECM, Lemos M, Filho JAX, Sennes LU, Saldiva PHN, Tsuji DH. Distribution of collagen in the lamina Propria of the human vocal fold. Laryngoscope 2003;113:2187-2191.
Gray SD, Titze IR, Alipour F, Hammond TH. Biomechanical and histologic observations of vocal fold fibrous proteins. Ann Otol Rhinol Laryngol 2000;109:77-85.
Ushiki T. Collagen fibers, reticular fibers and elastic fibers. A comprehensive understanding from a morphological viewpoint. Arch Histol Cytol 2002;65:109-126.
Fayoux P, Devisme L, Chevalier D, Merrot O, Gosselin B. Histologic structure and development of the laryngeal macula flava. Ann Otol Rhinol Laryngol 2004;113:498-504.
Hammond TH, Zhou R, Hammond EH, Pawlak A, Gray SD. The intermediate layer: a morphologic study of the elastin and hyaluronic acid constituents of normal human vocal folds. J Voice 1997;11:59-66.
Hammond TH, Gray SD, Butler JE. Age- and gender-related collagen distribution in human vocal folds. Ann Otol Rhinol Laryngol 2000;109:913-920.
Hirano M. Phonosurgery; basic & clinical investigations. Otologia 1975;1:239-442.
Sato K, Hirano M. Age-related changes of elastic fibers in the superficial layer of the lamina propria of vocal folds. Ann Otol Rhinol Laryngol 1997;106:44-48.
Finck C. Vocal fold structure and speech pathologies. Rev Laryngol Otol Rhinol (Bord) 2005;126:295-300.
Zhang Z. Mechanics of human voice production and control. J Acoust Soc Am 2016;140:2614-2635.
Thibeault SL, Gray SD, Bless DM, Chan RW, Ford CN. Histologic and rheologic characterization of vocal fold scarring. J Voice 2002;16:96-104.
Gunter HE. A mechanical model of vocal-fold collision with high spatial and temporal resolution. J Acoust Soc Am 2003;113:994-1000.
Jiang JJ, Titze IR. Measurement of vocal fold intraglottal pressure and impact stress. J Voice 1994;8:132-144.
Sato K, Hirano M. Histologic investigation of the macula flava of the human newborn vocal fold. Ann Otol Rhinol Laryngol 1995;104:556-562.
Ishii K, Akita M, Yamashita K, Hirose H. Age-related development of the arrangement of connective tissue fibers in the lamina propria of the human vocal fold. Ann Otol Rhinol Laryngol 2000;109:1055-1064.
Boseley ME, Hartnick CJ. Development of the human true vocal fold: depth of cell layers and quantifying cell types within the lamina propria. 2006;115:784-788.
Hartnick CJ, Rehbar R, Prasad V. Development and maturation of the pediatric human vocal fold lamina Propria. Laryngoscope 2005;115:4-15.
Nita LM, Battlehner CN, Ferreira MA, et al. The presence of a vocal ligament in fetuses: a histochemical and ultrastructural study. J Anat 2009;215:692-697.
De Campos D, Ellwanger JH, da Costa Rosa JP, et al. Morphology of fetal vocal fold and associated structures. J Voice 2013;27:5-10.
Rogers DJ, Setlur J, Raol N, Maurer R, Hartnick CJ. Evaluation of true vocal fold growth as a function of age. Otolaryngol Head Neck Surg 2014;151:681-686. https://doi.org/10.1177/0194599814547489.
Huang D, Swanson EA, Lin CP, et al. Optical coherence tomography. Science (80-) 1991;254:1178-1181.
Boudoux C, Leuin SC, Oh WY, et al. Preliminary evaluation of noninvasive microscopic imaging techniques for the study of vocal fold development. J Voice 2009;23:269-276.
Boudoux C, Benboujja F, Deterre R, Strupler M, Garcia J, Hartnick CJ. Emerging microscopy techniques for pediatric vocal fold evaluation. In: Izdebski K, Yan Y, Ward R, Wong BJF, eds. Normal & Abnormal Vocal Folds Kinematics: High-Speed Digital Phonoscopy (HSDP), Optical Coherence Tomography (OCT) & Narrow Band Imaging (NBI); 1st ed., Vol. 2. San Francisco, California & Oakland, California: PVSF e-Q&A-b; 2016:349-360.
Benboujja F, Garcia JA, Beaudette K, Strupler M, Hartnick CJ, Boudoux C. Intraoperative imaging of pediatric vocal fold lesions using optical coherence tomography. J Biomed Opt 2016;21:016007. https://doi.org/10.1117/1.JBO.21.1.016007.
Benboujja F, Hartnick C. Clinical and surgical implications of intraoperative optical coherence tomography imaging for benign pediatric vocal fold lesions. Int J Pediatr Otorhinolaryngol 2018;114:111-119.
Benboujja F, Bowe S, Boudoux C, Hartnick C. Utility of optical coherence tomography for guiding laser therapy among patients with recurrent respiratory papillomatosis. JAMA Otolaryngol Head Neck Surg 2018;144:831-837.
Wong BJF, Jackson RP, Guo S, et al. In vivo optical coherence tomography of the human larynx: normative and benign pathology in 82 patients. Laryngoscope 2005;115:1904-1911.
Ridgway JM, Ahuja G, Guo S, et al. Imaging of the pediatric airway using optical coherence tomography. Laryngoscope 2007;117:2206-2212.
Liu G, Rubinstein M, Saidi A, et al. Imaging vibrating vocal folds with a high speed 1050 nm swept source OCT and ODT. Opt Express 2011;19:11880-11889.
Volgger V, Sharma GK, Jing JC, et al. Long-range Fourier domain optical coherence tomography of the pediatric subglottis. Int J Pediatr Otorhinolaryngol 2015;79:119-126.
Sharma GK, Chin Loy A, Su E, et al. Quantitative evaluation of adult subglottic stenosis using intraoperative long-range optical coherence tomography. Ann Otol Rhinol Laryngol 2016;125:815-822.
Ridgway JM, Su J, Wright R, et al. Optical coherence tomography of the newborn airway. Ann Otol Rhinol Laryngol 2008;117:327-334.
Burns JA, Kim KH, Kobler JB, De Boer JF, Lopez-Guerra G, Zeitels SM. Real-time tracking of vocal fold injections with optical coherence tomography. Laryngoscope 2009;119:2182-2186.
Sato K, Umeno H, Nakashima T. Functional histology of the macula flava in the human vocal fold-part 2: its role in the growth and development of the vocal fold. Folia Phoniatr Logop 2010;62:263-270.
Hirano M, Kurita S, Sakaguchi S. Ageing of the vibratory tissue of human vocal folds. Acta Otolaryngol 1989;107:428-433.
Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012;9:676-682.
Tearney GJ, Brezinski ME, Bouma BE, Hee MR, Southern JF, Fujimoto JG. Determination of the refractive index of highly scattering human tissue by optical coherence tomography. Opt Lett 1995;20:2258.
Dowdall JR, Sadow PM, Hartnick C, et al. Identification of distinct layers within the stratified squamous epithelium of the adult human true vocal fold. Laryngoscope 2015;125:E313-E319.
Kimura M, Tayama N, Chan RW. Geometrical deformation of vocal fold tissues induced by formalin fixation. Laryngoscope 2003;113:607-613.
Buhler RB, Sennes LU, Mauad T, Melo ECM, Silva LFF, Saldiva PHN. Collagen fiber and versican distribution within the lamina propria of fetal vocal folds. Laryngoscope 2008;118:371-374.
Bühler RB, Sennes LU, Tsuji DH, Mauad T, da Silva LF, Saldiva PN. Collagen type I, collagen type III, and versican in vocal fold lamina propria. Arch Otolaryngol Head Neck Surg 2011;137:604-608.
Tucker JA, Vidic B, Tucker GF, Stead J. Survey of the development of laryngeal epithelium. Ann Otol Rhinol Laryngol 1976;85:3-16.
Teller SS, AJE F, Xiao L, et al. High-frequency viscoelastic shear properties of vocal fold tissues: implications for vocal fold tissue engineering. Tissue Eng Part A 2012;18:2008-2019.
Brodnitz FS. Hormones and the human voice. Bull New York Acad Med J Urban Heal 1971;47:183-191.
Abitbol J, Abitbol P, Abitbol B. Sex hormones and the female voice. J Voice 1999;13:424-446.
Sato K, Hirano M, Nakashima T. Comparative histology of the maculae flavae of the vocal folds. Ann Otol Rhinol Laryngol 2000;109:136-140.
Gray SD. Cellular physiology of the vocal volds. Otolaryngol Clin North Am 2000;33:679-697.
Enver N. A morphometric analysis of laryngeal anatomy: a cadaveric study. Turkish J Ear Nose Throat 2018;28:71-77.
Roberts T, Morton R, Al-Ali S. Microstructure of the vocal fold in elderly humans. Clin Anat 2011;24:544-551.
Maturo S, Benboujja F, Boudoux C, Hartnick C. Quantitative distinction of unique vocal fold subepithelial architectures using optical coherence tomography. Ann Otol Rhinol Laryngol 2012;121:754-760.
Benboujja F, Hartnick C. Quantitative evaluation of the human vocal fold extracellular matrix using multiphoton microscopy and optical coherence tomography. Sci Rep 2021;11:1-16.
Liu L, Gardecki JA, Nadkarni SK, et al. Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography. Nat Med 2011;17:1010-1014.
Boudoux C, Leuin SC, Oh WY, et al. Optical microscopy of the pediatric vocal fold. Arch Otolaryngol Head Neck Surg 2009;135:53-64.
Everett MJ, Schoenenberger K, Colston BW, Da Silva LB. Birefringence characterization of biological tissue by use of optical coherence tomography. Opt Lett 1998;23:228-230.
Burns JA, Kim KH, de Boer JF, Anderson RR, Zeitels SM. Polarization-sensitive optical coherence tomography imaging of benign and malignant laryngeal lesions: an in vivo study. Otolaryngol Head Neck Surg 2011;145:91-99.
Helmchen F, Denk W. Deep tissue two-photon microscopy. Nat Methods 2005;2:932-940.
Chen X, Nadiarynkh O, Plotnikov S, Campagnola PJ. Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protoc 2012;7:654-669.
Maturo S, Hill C, Bunting G, Ballif C, Maurer R, Hartnick C. Establishment of a normative pediatric acoustic database. Arch Otolaryngol Head Neck Surg 2012;138:956-961. https://doi.org/10.1001/2013.jamaoto.104.