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Preterm birth disrupts the development of feeding and breathing coordination.

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.

SUBMITTER: Mayerl CJ

PROVIDER: S-EPMC6620663 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Preterm birth disrupts the development of feeding and breathing coordination.

Mayerl Christopher J CJ Gould Francois D H FDH Bond Laura E LE Stricklen Bethany M BM Buddington Randal K RK German Rebecca Z RZ

Journal of applied physiology (Bethesda, Md. : 1985) 20190425 6

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 ...[more]

PMID: 31018743

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Project description:BackgroundWhen sufficient maternal breast milk is not available, alternative forms of enteral nutrition for preterm or low birth weight (LBW) infants are donor breast milk or artificial formula. Donor breast milk may retain some of the non-nutritive benefits of maternal breast milk for preterm or LBW infants. However, feeding with artificial formula may ensure more consistent delivery of greater amounts of nutrients. Uncertainty exists about the balance of risks and benefits of feeding formula versus donor breast milk for preterm or LBW infants.ObjectivesTo determine the effect of feeding with formula compared with donor breast milk on growth and development in preterm or low birth weight (LBW) infants.Search methodsWe used the Cochrane Neonatal search strategy, including electronic searches of the Cochrane Central Register of Controlled Trials (CENTRAL; 2017, Issue 6), Ovid MEDLINE, Embase, and the Cumulative Index to Nursing and Allied Health Literature (until 8 June 2017), as well as conference proceedings and previous reviews.Selection criteriaRandomised or quasi-randomised controlled trials (RCTs) comparing feeding with formula versus donor breast milk in preterm or LBW infants.Data collection and analysisTwo review authors assessed trial eligibility and risk of bias and extracted data independently. We analysed treatment effects as described in the individual trials and reported risk ratios (RRs) and risk differences (RDs) for dichotomous data, and mean differences (MDs) for continuous data, with respective 95% confidence intervals (CIs). We used a fixed-effect model in meta-analyses and explored potential causes of heterogeneity in subgroup analyses. We assessed the quality of evidence for the main comparison at the outcome level using "Grading of Recommendations Assessment, Development and Evaluation" (GRADE) methods.Main resultsEleven trials, in which 1809 infants participated in total, fulfilled the inclusion criteria. Four trials compared standard term formula versus donor breast milk and seven compared nutrient-enriched preterm formula versus donor breast milk. Only the four most recent trials used nutrient-fortified donor breast milk. The trials contain various weaknesses in methodological quality, specifically concerns about allocation concealment in four trials and lack of blinding in most of the trials.Formula-fed infants had higher in-hospital rates of weight gain (mean difference (MD) 2.51, 95% confidence interval (CI) 1.93 to 3.08 g/kg/day), linear growth (MD 1.21, 95% CI 0.77 to 1.65 mm/week) and head growth (MD 0.85, 95% CI 0.47 to 1.23 mm/week). We did not find evidence of an effect on long-term growth or neurodevelopment. Formula feeding increased the risk of necrotising enterocolitis (typical risk ratio (RR) 1.87, 95% CI 1.23 to 2.85; risk difference (RD) 0.03, 95% CI 0.01 to 0.06).The GRADE quality of evidence was moderate for rates of weight gain, linear growth, and head growth (downgraded for high levels of heterogeneity) and was moderate for neurodevelopmental disability, all-cause mortality, and necrotising enterocolitis (downgraded for imprecision).Authors' conclusionsIn preterm and LBW infants, feeding with formula compared with donor breast milk, either as a supplement to maternal expressed breast milk or as a sole diet, results in higher rates of weight gain, linear growth, and head growth and a higher risk of developing necrotising enterocolitis. The trial data do not show an effect on all-cause mortality, or on long-term growth or neurodevelopment.

Project description:BackgroundWhen sufficient maternal breast milk is not available, alternative forms of enteral nutrition for preterm or low birth weight (LBW) infants are donor breast milk or artificial formula. Donor breast milk may retain some of the non-nutritive benefits of maternal breast milk for preterm or LBW infants. However, feeding with artificial formula may ensure more consistent delivery of greater amounts of nutrients. Uncertainty exists about the balance of risks and benefits of feeding formula versus donor breast milk for preterm or LBW infants.ObjectivesTo determine the effect of feeding with formula compared with donor breast milk on growth and development in preterm or low birth weight (LBW) infants.Search methodsWe used the Cochrane Neonatal search strategy, including electronic searches of the Cochrane Central Register of Controlled Trials (CENTRAL; 2019, Issue 5), Ovid MEDLINE, Embase, and the Cumulative Index to Nursing and Allied Health Literature (3 May 2019), as well as conference proceedings, previous reviews, and clinical trials.Selection criteriaRandomised or quasi-randomised controlled trials (RCTs) comparing feeding with formula versus donor breast milk in preterm or LBW infants.Data collection and analysisTwo review authors assessed trial eligibility and risk of bias and extracted data independently. We analysed treatment effects as described in the individual trials and reported risk ratios (RRs) and risk differences (RDs) for dichotomous data, and mean differences (MDs) for continuous data, with respective 95% confidence intervals (CIs). We used a fixed-effect model in meta-analyses and explored potential causes of heterogeneity in subgroup analyses. We assessed the certainty of evidence for the main comparison at the outcome level using GRADE methods.Main resultsTwelve trials with a total of 1879 infants fulfilled the inclusion criteria. Four trials compared standard term formula versus donor breast milk and eight compared nutrient-enriched preterm formula versus donor breast milk. Only the five most recent trials used nutrient-fortified donor breast milk. The trials contain various weaknesses in methodological quality, specifically concerns about allocation concealment in four trials and lack of blinding in most of the trials. Most of the included trials were funded by companies that made the study formula.Formula-fed infants had higher in-hospital rates of weight gain (mean difference (MD) 2.51, 95% confidence interval (CI) 1.93 to 3.08 g/kg/day), linear growth (MD 1.21, 95% CI 0.77 to 1.65 mm/week) and head growth (MD 0.85, 95% CI 0.47 to 1.23 mm/week). These meta-analyses contained high levels of heterogeneity. We did not find evidence of an effect on long-term growth or neurodevelopment. Formula feeding increased the risk of necrotising enterocolitis (typical risk ratio (RR) 1.87, 95% CI 1.23 to 2.85; risk difference (RD) 0.03, 95% CI 0.01 to 0.05; number needed to treat for an additional harmful outcome (NNTH) 33, 95% CI 20 to 100; 9 studies, 1675 infants).The GRADE certainty of evidence was moderate for rates of weight gain, linear growth, and head growth (downgraded for high levels of heterogeneity) and was moderate for neurodevelopmental disability, all-cause mortality, and necrotising enterocolitis (downgraded for imprecision).Authors' conclusionsIn preterm and LBW infants, moderate-certainty evidence indicates that feeding with formula compared with donor breast milk, either as a supplement to maternal expressed breast milk or as a sole diet, results in higher rates of weight gain, linear growth, and head growth and a higher risk of developing necrotising enterocolitis. The trial data do not show an effect on all-cause mortality, or on long-term growth or neurodevelopment.

Project description:Swallowing in mammals requires the precise coordination of multiple oropharyngeal structures, including the palatopharyngeal arch. During a typical swallow, the activity of the palatopharyngeus muscle produces pharyngeal shortening to assist in producing pressure required to swallow and may initiate epiglottal flipping to protect the airway. Most research on the role of the palatopharyngeal arch in swallowing has used pharyngeal manometry, which measures the relative pressures in the oropharynx, but does not quantify the movements of the structures involved in swallowing. In this study, we assessed palatopharyngeal arch and soft palate function by comparing their movements in a healthy population to a pathophysiological population longitudinally through infancy (term versus preterm pigs). In doing so, we test the impact of birth status, postnatal maturation, and their interaction on swallowing. We tracked the three-dimensional (3D) movements of radiopaque beads implanted into relevant anatomical structures and recorded feeding via biplanar high-speed videofluoroscopy. We then calculated the total 3D excursion of the arch and soft palate, the orientation of arch movement, and the timing of maximal arch constriction during each swallow. Soft palate excursion was greater in term infants at both 7 and 17 days postnatal, whereas arch excursion was largely unaffected by birth status. Maximal arch constriction occurred much earlier in preterm pigs relative to term pigs, a result that was consistent across age. There was no effect of postnatal age on arch or soft palate excursion. Preterm and term infants differed in their orientation of arch movement, which most likely reflects both differences in anatomy and differences in feeding posture. Our results suggest that the timing and coordination of oropharyngeal movements may be more important to feeding performance than the movements of isolated structures, and that differences in the neural control of swallowing and its maturation in preterm and term infants may explain preterm swallowing deficits.

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Preterm birth disrupts the development of feeding and breathing coordination.

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Preterm birth disrupts the development of feeding and breathing coordination.

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