Literature DB >> 31018743

Preterm birth disrupts the development of feeding and breathing coordination.

Christopher J Mayerl1, Francois D H Gould1, Laura E Bond1, Bethany M Stricklen1, Randal K Buddington2, Rebecca Z German1.   

Abstract

All mammals must breathe and breathe continuously from birth. Similarly, all mammals, including infants, have high functional demands for feeding. However, the pathway that food takes through the pharynx interrupts respiration. The coordination between swallowing and breathing is therefore critical for all infant mammals. Clinically, this coordination differs between term and preterm infants. However, the neurological mechanisms underlying this coordination and how it matures as infants grow are poorly understood. Here, we integrate high-resolution data from multiple physiologic processes across a longitudinal time frame to study suck-swallow-breathe dynamics in a preterm animal model, the infant pig. In doing so, we test the hypothesis that preterm birth will have an impact on some, but not all, behaviors associated with suck-swallow-breath performance. We hypothesize that coordination will be disrupted, reflecting incomplete connections in the brainstem. We found that preterm pigs became rhythmic and mature in sucking and swallowing behaviors, suggesting substantial postnatal maturation in the coordination of these behaviors. However, their ability to coordinate swallowing and breathing never developed. These results have implications for the nature of clinical care of human infants, as well as for how feeding processes develop in mammals. Clinically, they provide a foundation for developing interventions for preterm infants. Additionally, these results suggest that the lack of coordination between swallowing and breathing may be a significant factor in determining the minimum gestation time across mammals. NEW & NOTEWORTHY Preterm infants face a variety of challenges associated with safe feeding, but obtaining high-resolution longitudinal data to understand these challenges in humans is challenging. We used a pig model to acquire high-speed videofluoroscopic and respiratory inductance plethysmograph data throughout the nursing period to show that preterm birth does not have substantial impacts on the ability of infants to perform isolated behaviors. However, it does decrease the ability of preterm infants to coordinate among behaviors during feeding.

Entities:  

Keywords:  aerodigestive; dysphagia; feeding; neonate; premature

Mesh:

Year:  2019        PMID: 31018743      PMCID: PMC6620663          DOI: 10.1152/japplphysiol.00101.2019

Source DB:  PubMed          Journal:  J Appl Physiol (1985)        ISSN: 0161-7567


  29 in total

1.  Developmental patterns of rhythmic suck and swallow in preterm infants.

Authors:  I H Gewolb; F L Vice; E L Schwietzer-Kenney; V L Taciak; J F Bosma
Journal:  Dev Med Child Neurol       Date:  2001-01       Impact factor: 5.449

2.  Abnormal lung function in healthy preterm infants.

Authors:  Ola Hjalmarson; Kenneth Sandberg
Journal:  Am J Respir Crit Care Med       Date:  2002-01-01       Impact factor: 21.405

3.  Emergence of oropharyngeal, laryngeal and swallowing activity in the developing fetal upper aerodigestive tract: an ultrasound evaluation.

Authors:  Jeri L Miller; Barbara C Sonies; Christian Macedonia
Journal:  Early Hum Dev       Date:  2003-02       Impact factor: 2.079

4.  Coordination of suck-swallow and swallow respiration in preterm infants.

Authors:  C Lau; E O Smith; R J Schanler
Journal:  Acta Paediatr       Date:  2003-06       Impact factor: 2.299

5.  Maturational changes in the rhythms, patterning, and coordination of respiration and swallow during feeding in preterm and term infants.

Authors:  Ira H Gewolb; Frank L Vice
Journal:  Dev Med Child Neurol       Date:  2006-07       Impact factor: 5.449

Review 6.  The neurobiology of swallowing and dysphagia.

Authors:  Arthur J Miller
Journal:  Dev Disabil Res Rev       Date:  2008

7.  Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited.

Authors:  A J Thexton; A W Crompton; R Z German
Journal:  J Appl Physiol (1985)       Date:  2006-11-02

8.  Volume and rate of milk delivery as determinants of swallowing in an infant model animal (Sus scrofia).

Authors:  Rebecca Z German; Alfred W Crompton; Tomasz Owerkowicz; Allan J Thexton
Journal:  Dysphagia       Date:  2004       Impact factor: 3.438

9.  Integration of the reflex pharyngeal swallow into rhythmic oral activity in a neurologically intact pig model.

Authors:  Rebecca Z German; A W Crompton; Allan J Thexton
Journal:  J Neurophysiol       Date:  2009-06-10       Impact factor: 2.714

10.  Maturation of oral feeding skills in preterm infants.

Authors:  N Amaizu; Rj Shulman; Rj Schanler; C Lau
Journal:  Acta Paediatr       Date:  2007-12-03       Impact factor: 2.299

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  15 in total

1.  Oropharyngeal capsaicin exposure improves infant feeding performance in an animal model of superior laryngeal nerve damage.

Authors:  Chloe E Edmonds; Rebecca Z German; Laura E Bond; Christopher J Mayerl
Journal:  J Neurophysiol       Date:  2022-07-13       Impact factor: 2.974

2.  Sucking versus swallowing coordination, integration, and performance in preterm and term infants.

Authors:  Christopher J Mayerl; Chloe E Edmonds; Emily A Catchpole; Alexis M Myrla; Francois D H Gould; Laura E Bond; Bethany M Stricklen; Rebecca Z German
Journal:  J Appl Physiol (1985)       Date:  2020-10-15

3.  Swallow Safety in Infant Pigs With and Without Recurrent Laryngeal Nerve Lesion.

Authors:  Bethany M Stricklen; Laura E Bond; Francois D H Gould; Rebecca Z German; Christopher J Mayerl
Journal:  Dysphagia       Date:  2020-02-28       Impact factor: 3.438

4.  Swallow Safety is Determined by Bolus Volume During Infant Feeding in an Animal Model.

Authors:  Christopher J Mayerl; Alexis M Myrla; Francois D H Gould; Laura E Bond; Bethany M Stricklen; Rebecca Z German
Journal:  Dysphagia       Date:  2020-04-24       Impact factor: 3.438

5.  The contractile patterns, anatomy and physiology of the hyoid musculature change longitudinally through infancy.

Authors:  C J Mayerl; K E Steer; A M Chava; L E Bond; C E Edmonds; F D H Gould; B M Stricklen; T L Hieronymous; R Z German
Journal:  Proc Biol Sci       Date:  2021-03-10       Impact factor: 5.349

6.  Pathophysiology of aspiration in a unilateral SLN lesion model using quantitative analysis of VFSS.

Authors:  Maya Stevens; Christopher J Mayerl; Laura Bond; Rebecca Z German; Julie M Barkmeier-Kraemer
Journal:  Int J Pediatr Otorhinolaryngol       Date:  2020-11-24       Impact factor: 1.675

7.  Increased viscosity of milk during infant feeding improves swallow safety through modifying sucking in an animal model.

Authors:  Christopher J Mayerl; Chloe E Edmonds; Francois D H Gould; Rebecca Z German
Journal:  J Texture Stud       Date:  2021-04-05       Impact factor: 3.942

8.  The effect of preterm birth, recurrent laryngeal nerve lesion, and postnatal maturation on hyoid and thyroid movements, and their coordination in infant feeding.

Authors:  Christopher J Mayerl; Emily A Catchpole; Chloe E Edmonds; Francois D H Gould; Katlyn E McGrattan; Laura E Bond; Bethany M Stricklen; Rebecca Z German
Journal:  J Biomech       Date:  2020-04-12       Impact factor: 2.789

9.  Changes in the coordination between respiration and swallowing from suckling through weaning.

Authors:  Laura E Bond; Christopher J Mayerl; Bethany M Stricklen; Rebecca Z German; Francois D H Gould
Journal:  Biol Lett       Date:  2020-04-08       Impact factor: 3.812

Review 10.  Push versus gravity for intermittent bolus gavage tube feeding of preterm and low birth weight infants.

Authors:  Jennifer A Dawson; Ravinder Summan; Nadia Badawi; Jann P Foster
Journal:  Cochrane Database Syst Rev       Date:  2021-08-04
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