Vocal Folds Detect Ionic Perturbations on the Luminal Surface: An In Vitro Investigation

  • Mahalakshmi Sivasankar
    Correspondence
    Address correspondence and reprint requests to Mahalakshmi Sivasankar, PhD, Department of Speech, Language, and Hearing Sciences, Purdue University, G-2D, Heavilon Hall, 500 Oval Drive, West Lafayette, IN 47907.
    Affiliations
    Department of Speech, Language, and Hearing Sciences, Purdue University, West Lafayette, Indiana
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  • Kimberly V. Fisher
    Affiliations
    Department of Communication Sciences and Disorders, Northwestern University, Evanston, Illinois
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Published:February 07, 2007DOI:https://doi.org/10.1016/j.jvoice.2006.11.005

      Summary

      The homeostasis of fluid bathing the luminal surface of the vocal folds is important for phonation and laryngeal defense. Dehydration of the respiratory tract during mouth breathing can perturb the concentration of sodium and chloride ions in surface fluid. Exposure to dry air also increases the osmolarity of airway surface fluid. We hypothesized that viable vocal fold epithelium would detect changes in the ionic and osmotic composition of fluid on the luminal surface. Therefore, we examined bioelectric responses of vocal folds exposed to physiologically real, luminal ionic and osmotic challenges in vitro. The study used randomized factorial design with experimental and sham control groups. Fifty native ovine vocal folds were exposed to five challenges (ionic, osmotic, combined ionic-osmotic, and sham) on the luminal surface. Bioelectric measures of potential difference (PD), short-circuit current (ISC), and tissue resistance were assessed at prechallenge baseline, during challenge, and after removal of challenge. Ionic and combined ionic-osmotic challenges reduced PD and ISC (P<0.01). These reductions depended on the nature of the ionic challenge, were observed within 10 minutes, lasted for the duration of exposure, and were reversible after removal of the challenge. Conversely, sham or osmotic challenge did not alter bioelectric parameters over time (P>0.05). Viable ovine vocal fold epithelia detect ionic perturbations to the luminal surface. This sensitivity to luminal ionic challenge may be necessary to maintain the homeostasis of surface fluid.

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      References

        • Man S.P.
        • Adams G.K.
        • Proctor D.F.
        Effect of temperature, relative humidity, and mode of breathing on canine airway secretion.
        J Appl Physiol. 1979; 50: 613-620
        • Hirsch J.
        • Tokayer J.
        • Robinson M.
        • Sackner M.
        Effects of dry air and subsequent humidification on tracheal mucus velocity in dogs.
        J Appl Physiol. 1975; 39: 242-262
        • Boucher R.C.
        • Stutts M.J.
        • Bromberg P.A.
        • Gatzy J.T.
        Regional differences in airway surface liquid composition.
        J Appl Physiol. 1981; 50: 610-620
        • Chen B.
        • Yeates D.
        Ion transport and regulation of respiratory tract fluid output in dogs.
        J Appl Physiol. 2001; 90: 821-831
        • Jayaraman S.
        • Song Y.
        • Vetrivel L.
        • Shankar L.
        • Verkman A.
        Noninvasive in vivo fluorescence measurement of airway-surface liquid depth, salt concentration and pH.
        J Clin Invest. 2001; 107: 317-324
        • Freed A.
        • Davis M.
        Hyperventilation with dry air increases airway surface fluid osmolality in canine peripheral airways.
        Am J Respir Crit Care Med. 1999; 159: 1101-1107
        • Banner A.
        • Green J.
        • O'Connor M.
        Relation of respiratory water loss to coughing after exercise.
        N Engl J Med. 1984; 311: 883-886
        • Anderson S.
        • Holzer K.
        Exercise-induced asthma: is it the right diagnosis in elite athletes.
        J Allergy Clin Immunol. 2000; 106: 419-428
        • McFadden E.
        • Lenner A.
        • Strohi K.
        Postexercise airway rewarming and thermally induced asthma.
        J Clin Invest. 1986; 78: 18-25
        • Boucher R.C.
        Human airway ion transport: part 1.
        Am J Respir Crit Care Med. 1994; 150: 271-281
        • Willumsen N.
        • Davis C.
        • Boucher R.C.
        Selective response of human airway epithelia to luminal but not serosal solution hypertonicity.
        J Clin Invest. 1994; 94: 779-787
        • Dortch-Carnes J.
        • Van Scott M.
        • Fedan J.
        Changes in smooth muscle tone during osmotic challenge in relation to epithelial bioelectric events in guinea pig isolated trachea.
        J Pharmacol Exp Ther. 1999; 289: 911-917
        • Yankaskas J.R.
        • Gatzy J.T.
        • Boucher R.C.
        Effects of raised osmolarity on canine tracheal epithelial ion transport function.
        J Appl Physiol. 1987; 62: 2241-2245
        • Chen B.
        • Yeates D.
        Differentiation of ion-associated and osmotically driven water transport in canine airways.
        Am J Respir Crit Care Med. 2000; 162: 1715-1722
        • Sant'Ambrogio G.
        • Anderson J.
        • Sant'Ambrogio F.
        • Matthew O.
        Response of laryngeal receptors to water solutions of different osmolality and ionic composition.
        Respir Med. 1991; 85: 57-60
        • Bradley R.
        Sensory receptors of the larynx.
        Am J Med. 2000; 108: 47-50
        • Sivasankar M.
        • Fisher K.
        Oral breathing increases Pth and vocal effort by superficial drying of the vocal fold mucosa.
        J Voice. 2002; 16: 172-181
        • Sivasankar M.
        • Fisher K.
        Oral breathing challenge in participants with vocal attrition.
        J Speech Lang Hear Res. 2003; 46: 1416-1427
        • Gray S.D.
        Cellular physiology of the vocal folds.
        Otolaryngol Clin North Am. 2000; 33: 679-697
        • Hemler R.J.
        • Wienke G.H.
        • Dejonckere P.H.
        The effect of relative humidity of inhaled air on acoustic parameters of voice in normal subjects.
        J Voice. 1997; 11: 295-300
        • Jiang J.
        • Verdolini K.
        • Aquino B.
        • Ng J.
        • Hanson D.
        Effects of dehydration on phonation in excised canine larynges.
        Ann Otol Rhinol Laryngol. 2000; 109: 568-575
        • Roy N.
        • Tanner K.
        • Gray S.
        • Blomgren M.
        • Fisher K.
        An evaluation of the effects of three laryngeal lubricants on phonation threshold pressure (PTP).
        J Voice. 2003; 17: 331-342
        • Verdolini K.
        • Min Y.
        • Titze I.
        • et al.
        Biological mechanisms underlying voice changes due to dehydration.
        J Speech Lang Hear Res. 2002; 45: 268-282
        • Verdolini K.
        • Titze I.
        • Druker D.
        Changes in phonation threshold pressure with induced conditions of hydration.
        J Voice. 1990; 4: 142-151
        • Fisher K.
        • Telser A.
        • Phillips J.
        • Yeates D.
        Regulation of vocal fold transepithelial water fluxes.
        J Appl Physiol. 2001; 91: 1401-1411
        • Daviskas E.
        • Anderson S.
        • Brannan J.
        • Chan H.-K.
        • Eberl S.
        • Bautovich G.
        Inhalation of dry powder mannitol increases mucociliary clearance.
        Eur Respir J. 1997; 10: 2449-2454
        • Daviskas E.
        • Anderson S.
        • Eberl S.
        • Chan H.-K.
        • Bautovich G.
        Inhalation of dry powder mannitol improves the clearance of mucus in patients with bronchiectasis.
        Am J Respir Crit Care Med. 1999; 159: 1843-1848
        • Phillips J.
        • Wong L.
        • Yeates D.
        Bidirectional transepithelial water transport: measurement and governing mechanisms.
        Biophys J. 1999; 76: 869-877
        • Phillips J.
        • Yeates D.
        Bidirectional transepithelial water transport: chloride-dependent mechanisms.
        J Membr Biol. 2000; 175: 213-221
        • Winters S.
        • Yeates D.
        Roles of hydration, sodium and chloride in regulation of canine mucociliary transport system.
        J Appl Physiol. 1997; 83: 1360-1369
        • Welsch M.
        Electrolyte transport by airway epithelia.
        Physiol Rev. 1987; 67: 1143-1184
        • Sbarabti A.
        • Merigo F.
        • Benati D.
        • et al.
        Identification and characterization of a specific sensory epithelium in the rat larynx.
        J Comp Neurol. 2004; 475: 188-201
        • Man S.P.
        • Hulbert W.
        • Park S.
        • Thomson A.
        • Hogg J.
        Asymmetry of canine tracheal epithelium: osmotically induced changes.
        J Appl Physiol. 1984; 57: 1338-1346
        • Hirsh J.
        Altering airway surface liquid volume: inhalation therapy with amiloride and hyperosmotic agents.
        Adv Drug Deliv Rev. 2002; 54: 1445-1462
        • Winters S.
        • Yeates D.B.
        Interaction between ion transporters and the mucociliary transport system in dog and baboon.
        J Appl Physiol. 1997; 83: 1348-1359
        • Boucher R.C.
        Human airway ion transport: part 2.
        Am J Respir Crit Care Med. 1994; 150: 581-593
        • Bryan-Sisneros A.
        • Fraser S.
        • Suh Y.
        • Djamgoz M.
        Toxic effects of the beta-amyloid precursor protein C-terminus fragment and Na/Ca gradients.
        Neuroreport. 2000; 11: 3357-3360
        • Watson C.
        • Rowland M.
        • Warhurst G.
        Functional modelling of tight junctions in intestinal cell monolayers using polyethylene glycol.
        Am J Physiol. 2001; 281: 388-397
        • Nahum-Levy R.
        • Tam E.
        • Shavit S.
        • Benviste M.
        Glutamate but not glycine agonist affinity for NMDA receptorsis influenced by small cations.
        J Neurosci. 2002; 22: 2550-2560
        • Wang L.
        • Tiniakov R.
        • Yeates D.
        Peripheral opiodergic regulation of the tracheobronchial mucociliary transport system.
        J Appl Physiol. 2003; 94: 2375-2383
        • Moreno G.
        • Merino A.
        • Mercado A.
        • et al.
        Electroneutral Na-coupled cotransporter expression in the kidney during variations of NaCl and water metabolism.
        Hypertension. 1998; 31: 1002-1006
      1. Sivasankar M. Vocal fold response to luminal ionic and osmotic perturbations. Communication sciences and disorders [Ph.D.]. Evanston, IL: Northwestern University; 2005.

        • Titze I.
        Phonation threshold pressure: a missing link in glottal aerodynamics.
        J Acoust Soc Am. 1992; 91: 2926-2935
        • Jiang J.
        • Ng J.
        • Hanson D.
        The effects of rehydration on phonation in excised canine larynges.
        J Voice. 1999; 13: 51-59
        • Finkelhor B.K.
        • Titze I.R.
        • Durham P.L.
        The effects of viscosity changes in the vocal folds on the range of oscillation.
        J Voice. 1988; 1: 320-335
        • Mogi G.
        • Watanbe N.
        • Maeda S.
        • Umehara T.
        Laryngeal secretions: an immunochemical and immunohistological study.
        Acta Otolaryngol. 1979; 87: 124-141