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Dysphagia

pp 1–9 | Cite as

Reduced Coordination of Hyolaryngeal Elevation and Bolus Movement in a Pig Model of Preterm Infant Swallowing

  • Emily Catchpole
  • Laura Bond
  • Rebecca German
  • Christopher Mayerl
  • Bethany Stricklen
  • François D. H. GouldEmail author
Original Article

Abstract

Preterm infants often have dysphagia. Because reducing lifetime cumulative exposure to radiation in the context of diagnosis and treatment is a continuing goal of all medical fields which use X-ray imaging, efforts exist to reduce reliance on the gold standard diagnostic tool for dysphagia, VFSS. Alternatives, such as video of external hyolaryngeal movement using video recordings of the anterior surface of the neck, must be evaluated and validated against videofluoroscopy, a task for which non-human animal models are appropriate. In this study, we tested the hypotheses that (1) swallows could be identified equally well from video of external hyolaryngeal movement and bolus movement in videofluoroscopy, and that (2) the two measures would be tightly temporally linked in both term and preterm infant pigs. We recorded 222 swallows in simultaneous and precisely synchronized high-speed videofluoroscopy and high-speed camera films of 4 preterm and 3 term infant pigs drinking milk from a bottle. In term pigs, the two measures consistently identified the same swallows in each image stream. However, in preterm pigs there was a high rate of false positives (~ 10% per feeding sequence) and false negatives (~ 27% per feeding sequence). The timing of hyolaryngeal elevation (external video) and bolus movement (videofluoroscopy) was correlated and consistent in terms pigs, but not in preterm pigs. Magnitude of hyolaryngeal elevation was less in preterm pig swallows than term pig swallows. Absence of epiglottal inversion in preterm pigs was not linked to variation in the timing of the two swallow events. Video of external hyolaryngeal movement, though a reliable swallow indicator in term infant pigs, was unreliable in preterm infant pigs. The coordination of swallowing events differs in preterm and term infant pigs. More research is needed into the distinctive biomechanics of preterm infant pigs.

Keywords

Deglutition Dysphagia Premature Biomechanics Pig 

Notes

Funding

Grant support: NIH R01 HD088561 was provided to Rebecca German.

Supplementary material

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Supplementary material 1 (AVI 21680 kb)
455_2019_10033_MOESM2_ESM.avi (36.2 mb)
Supplementary material 2 (AVI 37067 kb)

References

  1. 1.
    Logemann JA. Role of the modified barium swallow in management of patients with dysphagia. Otolaryngol Neck Surg. 1997;116:335–8.CrossRefGoogle Scholar
  2. 2.
    Lefton-Greif MA, Arvedson JC. Pediatric feeding and swallowing disorders: state of health, population trends, and application of the international classification of functioning, disability, and health. Semin Speech Lang. 2007;28:161–5.CrossRefGoogle Scholar
  3. 3.
    Molfenter SM, Steele CM. Physiological variability in the deglutition literature: hyoid and laryngeal kinematics. Dysphagia. 2011;26:67–74.CrossRefGoogle Scholar
  4. 4.
    Gross A, Ohlemacher J, German R, Gould F. LVC timing in infant pig swallowing and the effect of safe swallowing. Dysphagia. 2018;33:51–62.CrossRefGoogle Scholar
  5. 5.
    Riley A, Miles A, Steele CM. An exploratory study of hyoid visibility, position, and swallowing-related displacement in a pediatric population. Dysphagia. 2019;34:248–56.CrossRefGoogle Scholar
  6. 6.
    Gewolb IH, Vice FL, Schweitzer-Kenney EL, Taciak VL, Bosma JF. Developmental patterns of rhythmic suck and swallow in preterm infants. Dev Med Child Neurol. 2001;43:22–7.CrossRefGoogle Scholar
  7. 7.
    McGrattan KE, Sivalingam M, Hasenstab KA, Wei L, Jadcherla SR. The physiologic coupling of sucking and swallowing coordination provides a unique process for neonatal survival. Acta Paediatr. 2016;105(7):790–7.CrossRefGoogle Scholar
  8. 8.
    Goldfield EC, Smith V, Buonomo C, Perez J, Larson K. Preterm infant swallowing of thin and nectar-thick liquids: changes in lingual-palatal coordination and relation to bolus transit. Dysphagia. 2013;28:234–44.CrossRefGoogle Scholar
  9. 9.
    Crompton AW, German RZ, Thexton AJ. Development of the movement of the epiglottis in infant and juvenile pigs. Zoology. 2008;111:339–49.CrossRefGoogle Scholar
  10. 10.
    CASPLO. Practice standards and guidelines for dysphagia interventions by speech language pathologists. Toronto: CASPLO; 2018.Google Scholar
  11. 11.
    Rappazzo CA, Turk CL. The videofluoroscopic swallow study: introduction, limitations, and challenges. In: Ongkasuwan J, Chiou EH, editors. Pediatric dysphagia—challenges and controversies [Internet]. Cham: Springer; 2018. p. 67–86.CrossRefGoogle Scholar
  12. 12.
    Henderson M, Miles A, Holgate V, Peryman S, Allen J. Application and verification of quantitative objective videofluoroscopic swallowing measures in a pediatric population with dysphagia. J Pediatr. 2016;178(200–205):e1.CrossRefGoogle Scholar
  13. 13.
    Goldfield EC, Buonomo C, Fletcher K, Perez J, Margetts S, Hansen A, et al. Premature infant swallowing: patterns of tongue-soft palate coordination based upon videofluoroscopy. Infant Behav Dev. 2010;33:209–18.CrossRefGoogle Scholar
  14. 14.
    Gewolb IH, Vice FL. Maturational changes in the rhythms, patterning, and coordination of respiration and swallow during feeding in preterm and term infants. Dev Med Child Neurol. 2006;48:589–94.CrossRefGoogle Scholar
  15. 15.
    German RZ, Crompton AW, Gould FDH, Thexton AJ. Animal models for dysphagia studies: what have we learnt so far. Dysphagia. 2017;32(1):73–7.CrossRefGoogle Scholar
  16. 16.
    Ballester A, Gould F, Bond L, Stricklen B, Ohlemacher J, Gross A, et al. Maturation of the coordination between respiration and deglutition with and without recurrent laryngeal nerve lesion in an animal model. Dysphagia. 2018;33:627–35.CrossRefGoogle Scholar
  17. 17.
    German RZ, Crompton AW, McCluskey C, Thexton AJ. Coordination between respiration and deglutition in a preterm infant mammal, Sus scrofa. Arch Oral Biol. 1996;41:619–22.CrossRefGoogle Scholar
  18. 18.
    Sangild PT, Thymann T, Schmidt M, Stoll B, Burrin DG, Buddington RK. Invited review: the preterm pig as a model in pediatric gastroenterology. J Anim Sci. 2013;91:4713–29.CrossRefGoogle Scholar
  19. 19.
    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.CrossRefGoogle Scholar
  20. 20.
    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.CrossRefGoogle Scholar
  21. 21.
    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.CrossRefGoogle Scholar
  22. 22.
    German RZ, Campbell-Malone R, Crompton AW, Ding P, Holman S, Konow N, et al. The concept of hyoid posture. Dysphagia. 2011;26:97.CrossRefGoogle Scholar
  23. 23.
    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.  https://doi.org/10.1007/s00455-016-9762-2.Google Scholar
  24. 24.
    Amaizu N, Shulman RJ, Schanler RJ, Lau C. Maturation of oral feeding skills in preterm infants. Acta Paediatr. 2008;97:61–7.CrossRefGoogle Scholar
  25. 25.
    Barlow SM, Lee J, Wang J, Oder A, Hall S, Knox K, et al. Frequency-modulated orocutaneous stimulation promotes non-nutritive suck development in preterm infants with respiratory distress syndrome or chronic lung disease. J Perinatol. 2014;34:136.CrossRefGoogle Scholar
  26. 26.
    DeLozier KR, Gould FDH, Ohlemacher J, Thexton AJ, German RZ. The impact of recurrent laryngeal nerve lesion on oropharyngeal muscle activity and sensorimotor integration in an infant pig model. J Appl Physiol. 2018;125:159–66.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.NEOMEDRootstownUSA
  2. 2.Department of Cell Biology and NeuroscienceRowan University School of Osteopathic MedicineStratfordUSA

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