Skip to main content
Log in

LVC Timing in Infant Pig Swallowing and the Effect of Safe Swallowing

  • Original Article
  • Published:
Dysphagia Aims and scope Submit manuscript

Abstract

Recurrent laryngeal nerve (RLN) injury in neonates, a complication of head and neck surgeries, leads to increased aspiration risk and swallowing dysfunction. The severity of resulting sequelae range from morbidity, such as aspiration pneumonia, to mortality from infection and failure to thrive. The timing of airway protective events including laryngeal vestibule closure (LVC) is implicated in aspiration. We unilaterally transected the RLN in an infant pig model to observe changes in the timing of swallowing kinematics with lesion and aspiration. We recorded swallows using high-speed video-fluoroscopic swallow studies (VFSS) and scored them using the Infant Mammalian Penetration and Aspiration Scale (IMPAS). We hypothesized that changes would occur in swallowing kinematics (1) between RLN lesion and control animals, and (2) among safe swallows (IMPAS 1), penetration swallows (IMPAS 3), and aspiration swallows (IMPAS 7). We observed numerous changes in timing following RLN lesion in safe and unsafe swallows, suggesting pervasive changes in the coordination of oropharyngeal function. The timing of LVC, posterior tongue, and hyoid movements differed between pre- and post-lesion in safe swallows. Posterior tongue kinematics differed for post-lesion swallows with penetration. The timing and duration of LVC and posterior tongue movement differed between aspiration swallows pre- and post-lesion. After lesion, safe swallows and swallows with aspiration differed in timing of LVC, laryngeal vestibule opening, and posterior tongue and hyoid movements. The timing of thyrohyoid muscle activity varied with IMPAS, but not lesion. Further study into the pathophysiology of RLN lesion-induced swallowing dysfunction is important to developing novel therapies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  1. Fink BR, Martin RW, Rohrmann CA. Biomechanics of the human epiglottis. Acta Otolaryngol. 1979;87:554–9.

    Article  CAS  PubMed  Google Scholar 

  2. Logemann JA, Kahrilas PJ, Cheng J, Pauloski BR, Gibbons PJ, Rademaker AW, et al. Closure mechanisms of laryngeal vestibule during swallow. Am J Physiol Gastrointest Liver Physiol. 1992;262:G338.

    Article  CAS  Google Scholar 

  3. Macrae P, Anderson C, Humbert I. Mechanisms of airway protection during chin-down swallowing. J Speech Lang Hear Res. 2014;57:1251–8.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Calvo I, Sunday KL, Macrae P, Humbert IA. Effects of chin-up posture on the sequence of swallowing events. Head Neck. 2017;39:947–59.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Inamoto Y, Saitoh E, Okada S, Kagaya H, Shibata S, Ota K, et al. The effect of bolus viscosity on laryngeal closure in swallowing: kinematic analysis using 320-row area detector CT. Dysphagia. 2013;28:33–42.

    Article  PubMed  Google Scholar 

  6. Molfenter SM, Steele CM. Physiological variability in the deglutition literature: hyoid and laryngeal kinematics. Dysphagia. 2011;26:67–74.

    Article  PubMed  Google Scholar 

  7. Young JL, Macrae P, Anderson C, Taylor-Kamara I, Humbert IA. The sequence of swallowing events during the chin-down posture. Am J Speech Lang Pathol. 2015;24:659–70.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Gould FDH, Ohlemacher J, Lammers AR, Gross A, Ballester A, Fraley L, et al. Central nervous system integration of sensorimotor signals in oral and pharyngeal structures: oropharyngeal kinematics response to recurrent laryngeal nerve lesion. J Appl Physiol. 2016;120:495–502.

    Article  CAS  PubMed  Google Scholar 

  9. LaMantia A-S, Moody SA, Maynard TM, Karpinski BA, Zohn IE, Mendelowitz D, et al. Hard to swallow: developmental biological insights into pediatric dysphagia. Dev Biol. 2016;409:329–42.

    Article  CAS  PubMed  Google Scholar 

  10. Hersh C, Wentland C, Sally S, de Stadler M, Hardy S, Fracchia MS, et al. Radiation exposure from videofluoroscopic swallow studies in children with a type 1 laryngeal cleft and pharyngeal dysphagia: a retrospective review. Int J Pediatr Otorhinolaryngol. 2016;89:92–6.

    Article  PubMed  Google Scholar 

  11. German RZ, Crompton AW, Levitch LC, Thexton AJ. The mechanism of suckling in two species of infant mammal: miniature pigs and long-tailed macaques. J Exp Zool. 1992;261:322–30.

    Article  CAS  PubMed  Google Scholar 

  12. German RZ, Crompton AW, Gould FDH, Thexton AJ. Animal models for dysphagia studies: what have we learnt so far. Dysphagia. 2017. doi:10.1007/s00455-016-9778-7.

    PubMed Central  Google Scholar 

  13. Liu S-C, Chou Y-F, Su W-F. A rapid and accurate technique for the identification of the recurrent laryngeal nerve. Ann Otol Rhinol Laryngol. 2014;123:805–10.

    Article  PubMed  Google Scholar 

  14. Gould FDH, Lammers AR, Ohlemacher J, Ballester A, Fraley L, Gross A, et al. The physiologic impact of unilateral recurrent laryngeal nerve (RLN) lesion on infant oropharyngeal and esophageal performance. Dysphagia. 2015;30:714–22.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Alvarez-Berdugo D, Rofes L, Casamitjana JF, Padrón A, Quer M, Clavé P. Oropharyngeal and laryngeal sensory innervation in the pathophysiology of swallowing disorders and sensory stimulation treatments. Ann N Y Acad Sci. 2016;1380:104–20.

    Article  PubMed  Google Scholar 

  16. Thexton AJ, Crompton AW, German RZ. EMG activity in hyoid muscles during pig suckling. J Appl Physiol. 2012;112:1512–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Holman SD, Waranch DR, Campbell-Malone R, Ding P, Gierbolini-Norat EM, Lukasik SL, et al. Sucking and swallowing rates after palatal anesthesia: an electromyographic study in infant pigs. J Neurophysiol. 2013;110:387–96.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Holman SD, Campbell-Malone R, Ding P, Gierbolini-Norat EM, Lukasik SL, Waranch DR, et al. Swallowing kinematics and airway protection after palatal local anesthesia in infant pigs: swallowing after palatal anesthesia. Laryngoscope. 2014;124:436–45.

    Article  PubMed  Google Scholar 

  19. Thompson C, Donley E, Stimpson C, Horne W, Vinyard C. The influence of experimental manipulations on chewing speed during in vivo laboratory research in tufted capuchins (Cebus apella). Am J Phys Anthropol. 2011;145:402–14.

    Article  CAS  PubMed  Google Scholar 

  20. Gould FDH, Yglesias B, Ohlemacher J, German RZ. Pre-pharyngeal swallow effects of recurrent laryngeal nerve lesion on bolus shape and airway protection in an infant pig model. Dysphagia. 2016;32:362–73.

    Article  PubMed  Google Scholar 

  21. German RZ, Crompton AW, Thexton AJ. Integration of the reflex pharyngeal swallow into rhythmic oral activity in a neurologically intact pig model. J Neurophysiol. 2009;102:1017–25.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The lab would like to acknowledge the CMU staff and Biomechanical Journal Club. Special thanks to Dr. Vinyard and Dr. Young, as well as everyone who worked in the German laboratory.

Funding

This work was supported by NIH R01 DC9980 NIH R01 HD088561 to R.Z. German.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrew Gross.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gross, A., Ohlemacher, J., German, R. et al. LVC Timing in Infant Pig Swallowing and the Effect of Safe Swallowing. Dysphagia 33, 51–62 (2018). https://doi.org/10.1007/s00455-017-9832-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-017-9832-0

Keywords

Navigation