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Research Papers

Differences in the Microstructure and Biomechanical Properties of the Recurrent Laryngeal Nerve as a Function of Age and Location

[+] Author and Article Information
Megan J. Williams

Graduate Interdisciplinary Program of
Biomedical Engineering,
University of Arizona,
1130 North Mountain Avenue,
Tucson, AZ 85721
e-mail: mjoy@email.arizona.edu

Urs Utzinger

Department of Biomedical Engineering;
Graduate Interdisciplinary Program of
Biomedical Engineering,
University of Arizona,
Tucson, AZ 85721
BIO5 Institute,
University of Arizona,
Thomas W. Keating Bioresearch Building,
#131D, P.O. 210240,
Tucson, AZ 85721
e-mail: utzinger@email.arizona.edu

Julie M. Barkmeier-Kraemer

Voice and Swallowing Center,
The University of California—Davis,
2521 Stockton Blvd Suite 6200,
Sacramento, CA 95817
e-mail: jbark@ucdavis.edu

Jonathan P. Vande Geest

Associate Professor
Mem. ASME
Department of Aerospace and
Mechanical Engineering;
Department of Biomedical Engineering;
Graduate Interdisciplinary Program of
Biomedical Engineering,
University of Arizona,
Tucson, AZ 85721
BIO5 Institute,
University of Arizona,
Tucson, AZ 85721
e-mail: jpv1@email.arizona.edu

1Corresponding author.

Manuscript received January 22, 2014; final manuscript received April 30, 2014; accepted manuscript posted May 15, 2014; published online June 5, 2014. Assoc. Editor: Barclay Morrison.

J Biomech Eng 136(8), 081008 (Jun 05, 2014) (9 pages) Paper No: BIO-14-1044; doi: 10.1115/1.4027682 History: Received January 22, 2014; Revised April 30, 2014; Accepted May 15, 2014

Idiopathic onset of unilateral vocal fold paralysis (UVP) is caused by damage to the recurrent laryngeal nerve (RLN) and results in difficulty speaking, breathing, and swallowing. This damage may occur in this nerve as it loops around the aortic arch, which is in a dynamic biomechanical environment. The goal of this study is to determine if the location-dependent biomechanical and microstructural properties of the RLN are different in piglets versus adolescent pigs. The neck/distal and thoracic/proximal (near the aortic arch) regions of the RLN from eight adolescent pigs and six piglets were isolated and mechanically assessed in uni-axial tension. Two-photon imaging (second harmonic) data were collected at 5%, 10%, and 15% strain during the mechanical test. The tangential modulus (TM) and the strain energy density (W) were determined at each level of strain. The mean mode of the preferred fiber angle and the full width at half maximum (FWHM, a measure of fiber splay) were calculated from the imaging data. We found significantly larger values of TM, W, and FWHM in the proximal segments of the left RLN when compared to the distal segments (18.51 MPa ± 1.22 versus 10.78 MPa ± 1.22, p < 0.001 for TM, 0.046 MPa ± 0.01 versus 0.026 MPa ± 0.01, p < 0.003 for W, 15.52 deg ± 1.00 versus 12.98 deg ± 1.00, p < 0.001 for FWHM). TM and W were larger in the left segments than the right (15.32 MPa ± 1.20 versus 11.80 MPa ± 1.20, p < 0.002 for TM, 0.038 MPa ± 0.01 versus 0.028 MPa ± 0.01, p < 0.0001 for W). W was larger in piglets when compared to adolescent pigs (0.042 MPa ± 0.01 versus 0.025 MPa ± 0.01, p < 0.04). The proximal region of the left porcine RLN is more stiff than the distal region and has a higher degree of fiber splay. The left RLN of the adolescent pigs also displayed a higher degree of strain stiffening than the right. These differences may develop as a result of the more dynamic environment the left RLN is in as it loops around the aortic arch.

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References

Heitmiller, R. F., Tseng, E., and Jones, B., 2007, “Prevalence of Aspiration and Laryngeal Penetration in Patients With Unilateral Vocal Fold Motion Impairment,” Dysphagia, 15(4), pp. 184–187. [CrossRef]
Dedo, H. H., 1970, “The Paralyzed Larynx: An Electromyographic Study in Dogs and Humans,” Laryngoscope, 80(10), pp. 1455–1517. [CrossRef] [PubMed]
Duncan, I. D., Griffiths, I. R., McQueen, A., and Baker, G. O., 1974, “The Pathology of Equine Laryngeal Hemiplegia,” Acta Neuropathol., 27(4), pp. 337–348. [CrossRef] [PubMed]
Hillstrom, R. P., Cohn, A. M., and McCarroll, K. A., 1990, “Vocal Cord Paralysis Resulting From Neck Injections in the Intravenous Drug Use Population,” Laryngoscope, 100(5), pp. 503–506. [CrossRef] [PubMed]
Rosin, D. F., Handler, S. D., Potsic, W. P., Wetmore, R. F., and Tom, L. W. C., 1990, “Vocal Cord Paralysis in Children,” Laryngoscope, 100(11), pp. 1174–1179. [CrossRef] [PubMed]
Ward, P. H., and Berci, G., 1982, “Observations on So-Called Idiopathic Vocal Cord Paralysis,” Ann. Otol., Rhinol., Laryngol., 91(6 Pt 1), pp. 558–563.
Haller, J. M., Iwanik, M., and Shen, F. H., 2012, “Clinically Relevant Anatomy of Recurrent Laryngeal Nerve,” Spine, 37(2), pp. 97–100. [CrossRef] [PubMed]
Kelchner, L. N., Stemple, J. C., Gerdeman, E., Le Borgne, W., and Adam, S., 1999, “Etiology, Pathophysiology, Treatment Choices, and Voice Results for Unilateral Adductor Vocal Fold Paralysis: A 3-Year Retrospective,” J. Voice, 13(4), pp. 592–601. [CrossRef] [PubMed]
Mu, L., and Yang, S., 1991, “An Experimental Study on the Laryngeal Electromyography and Visual Observations in Varying Types of Surgical Injuries to the Unilateral Recurrent Laryngeal Nerve in the Neck,” Laryngoscope, 101(7 Pt 1), pp. 699–708. [CrossRef] [PubMed]
Quiney, R. E., and Michaels, L., 1990, “Histopathology of Vocal Cord Palsy From Recurrent Laryngeal Nerve Damage,” J. Otolaryngol., 19(4), pp. 237–241. [PubMed]
Sannella, N. A., Tober, R. L., Cipro, R. P., Pedicino, J. F., Donovan, E., and Gabriel, N., 1990, “Vocal Cord Paralysis Following Carotid Endarterectomy: The Paradox of Return of Function,” Ann. Vasc. Surg., 4(1), pp. 42–45. [CrossRef] [PubMed]
Teixido, M. T., and Leonetti, J. P.,1990, “Recurrent Laryngeal Nerve Paralysis Associated With Thoracic Aortic Aneurysm,” Otolaryngol., Head Neck Surg., 102(2), pp. 140–144.
Cunning, D. S., 1955, “Unilateral Vocal Cord Paralysis,” Ann. Otol., Rhinol., Laryngol., 64(2), pp. 487–493.
Huppler, E. G., Schmidt, H. W., Devine, D., and Gage, R. P., 1955, “Causes of Vocal-Cord Paralysis,” Proc. Staff Meet. Mayo Clin., 30(22), pp. 518–521.
Sulica, L., 2008, “The Natural History of Idiopathic Unilateral Vocal Fold Paralysis: Evidence and Problems,” Laryngoscope, 118(7), pp. 1303–1307. [CrossRef] [PubMed]
Bando, H., Nishio, T., Bamba, H., Uno, T., and Hisa, Y., 2006, “Vocal Fold Paralysis as a Sign of Chest Diseases: A 15-Year Retrospective Study,” World J. Surg., 30(3), pp. 293–298. [CrossRef] [PubMed]
Coscaron Blanco, E., Blanco Garcia, J. L., and Gomez Gonzalez, J. L., 2006, “An Uncommon Cause for Unilateral Vocal Fold Paralisis: Aortic Aneurysms. Case Report and Literature Review,” Otorrinolaringol. Ibero. Am., 33(5), pp. 481–487.
Escribano, J. F., Carnés, J., Crespo, M. A., and Antón, R. F., 2006, “Ortner's Syndrome and Endoluminal Treatment of a Thoracic Aortic Aneurysm: A Case Report,” Vasc. Endovasc. Surg., 40(1), pp. 75–78. [CrossRef]
Wunderlich, C., Wunderlich, O., Tausche, A. K., Fuhrmann, J., Boscheri, A., and Strasser, R. H., 2007, “Ortner's Syndrome or Cardiovocal Hoarseness,” Int. Med. J., 37(6), pp. 418–419. [CrossRef]
Lundborg, G., 1998, “Intraneural Microcirculation,” Orthop. Clin. North Am., 19(1), pp. 1–12.
Peters, A., Palay, S. L., and Webster, H. D., 1991, The Fine Structure of the Nervous System: Neurons and Their Supporting Cells, 3rd ed., Oxford University Press, NY,. p. 494.
Sunderland, S., 1965 “The Connective Tissues of Peripheral Nerves,” Brain, 88(4), pp. 841–854. [CrossRef] [PubMed]
Sunderland, S., 1970, “Anatomical Features of Nerve Trunks in Relation to Nerve Injury and Nerve Repair,” Clin. Neurosurg., 17, pp. 38–62. [PubMed]
Sunderland, S., 1978, Nerves and Nerve Injuries, 2nd ed., Churchill Livingstone; Longman, Edinburgh, p. 1046.
Sunderland, S., 1990, “The Anatomy and Physiology of Nerve Injury,” Muscle Nerve, 13(9), pp. 771–784. [CrossRef] [PubMed]
Sunderland, S., and Bradley, K. C., 1961, “Stress-Strain Phenomena in Denervated Peripheral Nerve Trunks,” Brain, 84, pp. 125–127. [CrossRef]
Sunderland, S., and Bradley, K. C., 1961, “Stress-Strain Phenomena in Human Peripheral Nerve Truanks,” Brain, 84, pp. 102–119. [CrossRef]
Sunderland, S., and Bradley, K. C., 1961, “Stress-Strain Phenomena in Human Spinal Nerve Roots,” Brain, 84, pp. 120–124. [CrossRef]
Thomas, P. K., 1963, “The Connective Tissue of Peripheral Nerve: An Electron Microscope Study,” J. Anat., 97, pp. 35–44. [PubMed]
Ushiki, T., and Ide, C., 1990, “Three-Dimensional Organization of the Collagen Fibrils in the Rat Sciatic Nerve as Revealed by Transmission- and Scanning Electron Microscopy,” Cell Tissue Res., 260(1), pp. 175–184. [CrossRef] [PubMed]
Haftek, J., 1970, “Stretch Injury of Peripheral Nerve. Acute Effects of Stretching on Rabbit Nerve,” J. Bone Jt. Surg. Br., 52(2), pp. 354–365.
Rydevik, B. L., Kwan, M. K., Myers, R. R., Brown, R. A., Triggs, K. J., Woo, S. L., and Garfin, S. R., 1990, “An in Vitro Mechanical and Histological Study of Acute Stretching on Rabbit Tibial Nerve,” J. Orthop. Res., 8(5), pp. 694–701. [CrossRef] [PubMed]
Nicholson, K. J., and Winkelstein, B. A., 2011, “Nerve and Nerve Root Biomechanics,” Neural Tissue Biomech., 3, pp. 203–229. [CrossRef]
Sunderland, S., and Bedbrook, G. M., 1949, “The Cross-Sectional Area of Peripheral Nerve Trunks Devoted to Nerve Fibres,” Brain, 72, pp. 428–449. [CrossRef] [PubMed]
Campbell, E. O., Samlan, R. A., McMullen, N. T., Cook, S., Smiley-Jewell, S., and Barkmeier-Kraemer, J., 2013, “Developmental Changes in the Connective Tissues of the Porcine Recurrent Laryngeal Nerve,” J. Anat., 222(6), pp. 625–633. [CrossRef] [PubMed]
Alexander, M. J., Barkmeier-Kraemer, J. M., and Vande Geest, J. P., 2010, “Biomechanical Properties of Recurrent Laryngeal Nerve in the Piglet,” Ann. Biomed. Eng., 38(8), pp. 2553–2562. [CrossRef] [PubMed]
Sunderland, S., 1945, “The Adipose Tissue of Peripheral Nerves,” Brain, 68, pp. 118–122. [CrossRef] [PubMed]
Sunderland, S., 1951, “A Classification of Peripheral Nerve Injuries Producing Loss of Function,” Brain, 74(4), pp. 491–516. [CrossRef] [PubMed]
Peti-Peterdi, J., and Bell, P. D., 2003, “Confocal and Two-Photon Microscopy,” Methods Mol. Med., 86, pp. 129–138. [CrossRef] [PubMed]
Kirkpatrick, N. D., Hoying, J. B., Botting, S. K., Weiss, J. A., and Utzinger, U., 2006, “In Vitro Model for Endogenous Optical Signatures of Collagen,” J. Biomed. Opt., 11(5), p. 054021. [CrossRef] [PubMed]
Raghavan, M. L., and Vorp, D. A., 2000, “Toward a Biomechanical Tool to Evaluate Rupture Potential of Abdominal Aortic Aneurysm: Identification of a Finite Strain Constitutive Model and Evaluation of Its Applicability,” J. Biomech., 33(4), pp. 475–482. [CrossRef] [PubMed]
Borschel, G. H., Kia, K. F., Kuzon, W. M., Jr., and Dennis, R. G., 2003, “Mechanical Properties of Acellular Peripheral Nerve,” J. Surg. Res., 114(2), pp. 133–139. [CrossRef] [PubMed]
Ma, Z., Hu, S., Tan, J. S., Myer, C., Njus, N. M., and Xia, Z., 2013, “In Vitro and in Vivo Mechanical Properties of Human Ulnar and Median Nerves,” J. Biomed. Mater. Res. A, 101(9), pp. 2718–2725. [CrossRef] [PubMed]
Millesi, H., Zoch, G., and Reihsner, R., 1995, “Mechanical Properties of Peripheral Nerves,” Clin. Orthop. Relat. Res., 1995(314), pp. 76–83.
Phillips, J. B., Smit, X., De Zoysa, N., Afoke, A., and Brown, R. A., 2004, “Peripheral Nerves in the Rat Exhibit Localized Heterogeneity of Tensile Properties During Limb Movement,” J. Physiol., 557(Pt 3), pp. 879–887. [CrossRef] [PubMed]
Rickett, T., Connell, S., Bastijanic, J., Hegde, S., and Shi, R., 2011, “Functional and Mechanical Evaluation of Nerve Stretch Injury,” J. Med. Syst., 35(5), pp. 787–793. [CrossRef] [PubMed]
Topp, K. S., and Boyd, B. S., 2006, “Structure and Biomechanics of Peripheral Nerves: Nerve Responses to Physical Stresses and Implications for Physical Therapist Practice,” Phys. Ther., 86(1), pp. 92–109. [PubMed]
Wall, E. J., Kwan, M. K., Rydevik, B. L., Woo, S. L., and Garfin, S. R., 1991, “Stress Relaxation of a Peripheral Nerve,” J. Hand Surg. Am., 16(5), pp. 859–863. [CrossRef] [PubMed]
Wall, E. J., Massie, J. B., Kwan, M. K., Rydevik, B. L., Myers, R. R., and Garfin, S. R., 1992, “Experimental Stretch Neuropathy. Changes in Nerve Conduction Under Tension,” J. Bone Jt. Surg. Br., 74(1), pp. 126–129.
Deslauriers, J., 2007, “Anatomy of the Neck and Cervicothoracic Junction,” Thoracic Surg. Clin.17, pp. 529–547. [CrossRef]

Figures

Grahic Jump Location
Fig. 1

Anatomy of the right and left recurrent laryngeal nerve and surrounding environment. This figure has been reprinted and adapted from Deslauriers, J., 2007, “Anatomy of the Neck and Cervicothoracic Junction,” Thoracic Surg. Clin. 17, pp. 529–544. Copyright 2007 by Elsevier, Inc. [50].

Grahic Jump Location
Fig. 2

Cauchy stress–stretch ratio data from a representative piglet specimen (a) and a representative adolescent pig specimen and (b) with corresponding fits with α and β values

Grahic Jump Location
Fig. 3

Representative SHG multiphoton images of a proximal segment of piglet RLN (left) and a proximal segment of adolescent pig RLN (right) at 0% strain (top) and 15% strain (middle). SHG channel depicts the collagen content of the tissue. These images are taken approximately 100 μm into the adolescent pig segment and 60 μm into the piglet segment. The red arrows indicate the angle at which 90 deg is measured. Histograms (bottom) show the overall collagen fiber orientations throughout the tissue at 0% and 15% strains.

Grahic Jump Location
Fig. 4

(a) Average TM is reported for adolescent and piglet nerves at each value of stretch; (b) average TM is reported for all adolescent and piglet RLN segments and all left and right RLN segments (*p < 0.002); and (c) average TM is reported for proximal and distal segments of the left and right RLN (*,†p < 0.001)

Grahic Jump Location
Fig. 5

(a) Average W is reported for adolescent and piglet nerves at each value of stretch; (b) average W is reported for all adolescent and piglet RLN segments (*p < 0.038) and all left and right RLN segments (†p < 0.001); (c) Average W is reported for all proximal and distal segments of adolescent pigs and piglets (‡,†p < 0.008; *,§p < 0.007); and (d) Average W is reported for all proximal and distal segments of the left and right RLN (*,†p < 0.002)

Grahic Jump Location
Fig. 6

(a) Average values of α and β are reported for all adolescent pig and piglet RLN segments (*p < 0.006, †p < 0.014); (b) average α is reported for all proximal and distal segments of the left and right RLN (*p < 0.011)

Grahic Jump Location
Fig. 7

(a) Average FWHM is reported for all proximal and distal segments of all left and right RLNs (†,*p < 0.004; ‡,§p < 0.001); (b) average mean mode is reported for all proximal and distal segments (*p < 0.004)

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