Skip to main content

Advertisement

SpringerLink
Log in

Variation in the Timing and Frequency of Sucking and Swallowing over an Entire Feeding Session in the Infant Pig Sus scrofa

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

Abstract

Feeding is a rhythmic behavior that consists of several component cycle types. How the timing of these cycles changes over a complete feeding sequence is not well known. To test the hypothesis that cycle frequency/duration changes as a function of time spent feeding, we examined complete feeding sequences in six infant pigs, using EMG of mylohyoid and thyrohyoid as cycle markers. We measured the instantaneous frequency of sucking and of swallowing cycles in 19 sequences. Each sequence contained three qualitatively distinctive phases of sucking frequency. Phase 1 started with cycles at a very high frequency and quickly dropped to a more constant level with low variation, which characterized phase 2. Phase 3 had a steady level of frequency but was interspersed with a number of high- or low-frequency cycles. Each phase differed from the others in patterns of within-phase variation and among-phase variation. Phase 2 had the least variation, and phase 3 had the largest range of frequencies. The number of sucks per swallow also differed among phases. These patterns, which characterize normative feeding, could indicate a physiologic basis in satiation. In human infant clinical studies, where data collection is often limited, these results indicated the utility of collecting data in different phases. Finally, these results can be used as a template or pattern with which to assess clinically compromised infants.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Arvedson JC. Assessment of pediatric dysphagia and feeding disorders: clinical and instrumental approaches. Dev Disabil Res Rev. 2008;14(2):118–27.

    Article  PubMed  Google Scholar 

  2. Book SA, Bustad LK. The fetal and neonatal pig in biomedical research. J Anim Sci. 1974;38(5):997–1002.

    CAS  PubMed  Google Scholar 

  3. Campbell-Malone R, et al. Ontogenetic changes in mammalian feeding: insights from electromyographic data. Integr Comp Biol. 2001;51(2):282–8.

    Article  Google Scholar 

  4. Chi-Fishman G, Sonies BC. Motor strategy in rapid sequential swallowing: new insights. J Speech Lang Hear Res. 2000;43(6):1481–92.

    Article  CAS  PubMed  Google Scholar 

  5. Crompton AW, Thexton AJ, German RZ. Development of the movement of the epiglottis in infant and juvenile pigs. Zoology. 2008;111:339–49.

    Article  PubMed Central  PubMed  Google Scholar 

  6. Delaney AL, Arvedson JC. Development of swallowing and feeding: prenatal through first year of life. Dev Disabil Res Rev. 2008;14(2):105–17.

    Article  PubMed  Google Scholar 

  7. Ding P, et al. Unilateral superior laryngeal nerve lesion in an animal model of dysphagia and its effect on sucking and swallowing. Dysphagia. 2013;28(3):404–12.

    Article  PubMed  Google Scholar 

  8. Ding P. The effect of unilateral superior laryngeal nerve lesion on swallowing threshold volume. Laryngoscope. 2013;123(8):1942–7.

    Article  PubMed  Google Scholar 

  9. Franks HA, Crompton AW, German RZ. Mechanism of intraoral transport in macaques. Am J Phys Anthropol. 1984;65(3):275–82.

    Article  CAS  PubMed  Google Scholar 

  10. Franks HA, et al. Mechanism of intraoral transport in a herbivore, the hyrax (Procavia syriacus). Arch Oral Biol. 1985;30(7):539–44.

    Article  CAS  PubMed  Google Scholar 

  11. German RZ, Crompton AW. Ontogeny of suckling mechanisms in opossums (Didelphis virginiana). Brain Behav Evol. 1996;48(3):157–64.

    Article  CAS  PubMed  Google Scholar 

  12. German RZ, Crompton AW. The Ontogeny of Feeding in Mammals. In: Schwenk K, editor. Feeding: Form, Function and Evolution in Tetrapod Vertebrates. San Diego: Academic Press; 2000. p. 449–57.

    Chapter  Google Scholar 

  13. German RZ, et al. Food transport through the anterior oral cavity in macaques. Am J Phys Anthropol. 1989;80(3):369–77.

    Article  CAS  PubMed  Google Scholar 

  14. German RZ, et al. Determinants of rhythm and rate in suckling. J Exp Zool. 1997;278:1–8.

    Article  CAS  PubMed  Google Scholar 

  15. German RZ, Crompton AW, Thexton AJ. The role of animal models in understanding feeding behavior in infants. Int J Orofacial Myology. 2004;30:20–30.

    CAS  PubMed  Google Scholar 

  16. 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(2):1017–25.

    Article  PubMed Central  PubMed  Google Scholar 

  17. Hiiemae KM. Feeding in Mammals. In: Schwenk K, editor. Feeding: form, function and evolution in tetrapod vertebrates. San Diego: Academic Press; 2000. p. 411–48.

    Chapter  Google Scholar 

  18. Hiiemae KM, Crompton AW. Mastication, food transport and swallowing. In: Hildebrand M, et al., editors. Functional Vertebrate Morphology. Cambridge: Harvard University Press; 1985. p. 262–90.

    Google Scholar 

  19. Hiiemae KM, Palmer JB. Food transport and bolus formation during complete feeding sequences on foods of different initial consistencies. Dysphagia. 1999;14(1):31–42.

    Article  CAS  PubMed  Google Scholar 

  20. Holman SD, et al. Regional variation in geniohyoid muscle strain during suckling in the infant pig. J Exp Zool A Ecol Genet Physiol. 2012;317(6):359–70.

    Article  PubMed  Google Scholar 

  21. Holman SD, Campbell-Malone R, et al. Development, reliability, and validation of an infant mammalian penetration-aspiration scale. Dysphagia. 2013;28(2):178–87.

    Article  PubMed Central  PubMed  Google Scholar 

  22. Holman SD, Waranch DR, et al. Sucking and swallowing rates after palatal anesthesia: an electromyographic study in infant pigs. J Neurophysiol. 2013;110(2):387–96.

    Article  PubMed Central  PubMed  Google Scholar 

  23. Holman SD, et al. Swallowing kinematics and airway protection after palatal local anesthesia in infant pigs. Laryngoscope. 2014;124(2):436–45.

    Article  PubMed  Google Scholar 

  24. Konow N, et al. Regional differences in length change and electromyographic heterogeneity in sternohyoid muscle during infant mammalian swallowing. J Appl Physiol. 2010;109:439–48.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Lefton-Greif MA, McGrath-Morrow SA. Deglutition and respiration: development, coordination, and practical implications. Semin Speech Lang. 2007;28(3):166–79.

    Article  PubMed  Google Scholar 

  26. Rommel N, et al. Development of pharyngo-esophageal physiology during swallowing in the preterm infant. Neurogastroenterol Motil. 2011;23(10):e401–8.

    Article  CAS  PubMed  Google Scholar 

  27. Sack WO. Pig anatomy and atlas. Ithaca: Veterinary Textbooks; 1982.

    Google Scholar 

  28. Thexton AJ, Crompton AW, German RZ. Electromyographic activity during the reflex pharyngeal swallow in the pig: doty and Bosma (1956) revisited. J Appl Physiol. 2007;102(2):587–600.

    Article  CAS  PubMed  Google Scholar 

  29. Thexton AJ, et al. Impact of rhythmic oral activity on the timing of muscle activation in the swallow of the decerebrate pig. J Neurophysiol. 2009;101(3):1386–93.

    Article  PubMed Central  PubMed  Google Scholar 

  30. Thexton AJ, Crompton AW, German RZ. EMG activity in hyoid muscles during pig suckling. J Appl Physiol (1985). 2012;112(9):1512–9.

    Article  CAS  Google Scholar 

  31. Weaver ME, Jump EB, McKean CF. The eruption pattern of permanent teeth in miniature swine. Arch Oral Biol. 1969;14(3):323–31.

    Article  CAS  PubMed  Google Scholar 

  32. Weckmueller J, Easterling C, Arvedson J. Preliminary temporal measurement analysis of normal oropharyngeal swallowing in infants and young children. Dysphagia. 2011;26(2):135–43.

    Article  PubMed  Google Scholar 

  33. Wentzel SE, Konow N, German RZ. Regional differences in hyoid muscle activity and length dynamics during mammalian head shaking. J Exp Zool A Ecol Genet Physiol. 2011;315(3):111–20.

    Article  PubMed  Google Scholar 

  34. Wykes LJ, Ball RO, Pencharz PB. Development and validation of a total parenteral nutrition model in the neonatal piglet. J Nutr. 1993;123(7):1248–59.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We appreciate Laurie Pipitone for her support during data collection. We also thank Melanie Albano and Kristy Koenig for their work during animal surgery. Stacey L. Lukasik and Regina Campbell-Malone provided thoughtful support and assistance during the whole study. Allan Thexton’s insights improved this article significantly. This study was funded by the National Institutes of Health (DC009980 to RZG).

Conflict of interest

None

Author information

Authors and Affiliations

  1. Department of Physical Medicine and Rehabilitation, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Estela M. Gierbolini-Norat, Shaina D. Holman, Peng Ding & Rebecca Z. German

  2. Department of Neural and Pain Sciences, University of Maryland School of Dentistry, 650 W Baltimore St, Baltimore, MD, USA

    Shaina D. Holman & Rebecca Z. German

  3. Department of Anatomy and Neurobiology, Northeast Ohio Medical University, 4209 SR 44, Rootstown,, OH 44272, USA

    Shubham Bakshi & Rebecca Z. German

Authors
  1. Estela M. Gierbolini-Norat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaina D. Holman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peng Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shubham Bakshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rebecca Z. German
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rebecca Z. German.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gierbolini-Norat, E.M., Holman, S.D., Ding, P. et al. Variation in the Timing and Frequency of Sucking and Swallowing over an Entire Feeding Session in the Infant Pig Sus scrofa . Dysphagia 29, 475–482 (2014). https://doi.org/10.1007/s00455-014-9532-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-014-9532-y

Keywords

Search

Navigation