Mammalian infants must be able to integrate the acquisition, transport, and swallowing of food in order to effectively feed. Understanding how these processes are coordinated is critical, as they have differences in neural control and sensitivity to perturbation. Despite this, most studies of infant feeding focus on isolated processes, resulting in a limited understanding of the role of sensorimotor integration in the different processes involved in infant feeding. This is especially problematic in the context of preterm infants, as they are considered to have a pathophysiological brain development and often experience feeding difficulties. Here, we use an animal model to study how the different properties of food acquisition, transport, and swallowing differ between term and preterm infants longitudinally through infancy in order to understand which processes are sensitive to variation in the bolus being swallowed. We found that term infants are better able to acquire milk than preterm infants, and that properties of acquisition are strongly correlated with the size of the bolus being swallowed. In contrast, behaviors occurring during the pharyngeal swallow, such as hyoid and soft palate movements, show little to no correlation with bolus size. These results highlight the pathophysiological nature of the preterm brain and also demonstrate that behaviors occurring during oral transport are much more likely to respond to sensory intervention than those occurring during the 'pharyngeal phase'.
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 movements of radiopaque beads implanted into relevant anatomical structures and recorded feeding via biplanar high-speed videofluoroscopy. We then calculated the total three-dimensional 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 seven 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.
Feeding in infant mammals requires the precise coordination of multiple oropharyngeal structures, including the palatopharyngeal arch. During a typical swallow, the activity of the palatopharyngeus muscle produces constriction of the arches and lowers the soft palate, which may be responsible for flipping of the epiglottis to cover the airway. Most research on the role of the palatopharyngeal arches in swallowing has been limited to pharyngeal manometry, which provides insight into the relative pressures in the oropharynx during swallowing. Studies using manometry in preterm infants, or in those with iatrogenic sequelae such as recurrent laryngeal nerve (RLN) damage, suggest differences in function, but not on how the structures in the oropharynx move to contribute to those changes in function. In this study, we assessed palatopharyngeal arch kinematics during feeding by using our validated infant pig model to determine the impact of birth status (preterm versus term), lesion status (lesioned RLN versus intact) and their interaction on feeding performance. We placed tantalum radio‐opaque beads into relevant anatomical structures of 16 infant pigs, including the palatopharyngeal arches, the tongue, the hard and soft palate, and the nose. We recorded feeding at both seven and 17 days postnatal via biplanar high‐speed videofluoroscopy (100fps) across a total of 584 swallows. Using XMALab, we tracked the three‐dimensional movement of the arches relative to a rigid body comprised of the markers in the hard palate and the nose. We then used custom MATLAB code to calculate the three‐dimensional excursion of the arches during a swallow, as well as the timing of constriction initiation, and the point of maximal constriction during a swallow. We found that preterm infants had more variable arch excursion than term infants, and RLN lesion increased excursion for both term and preterm infants although there were minimal differences in arch excursion within an age between term and preterm infants. Term infants also reached maximal arch constriction later than preterm infants, most likely due to their larger arch excursion and larger bolus volume. Lesion infants, both term and preterm, also had delayed maximal arch constriction during swallows, although day 17 term lesion infants reached maximal constriction earlier than term day 17 infants. Lesion resulted in delayed initiation of arch constriction, which did not change with age, although older term infants exhibited later arch constriction initiation than older preterm infants. Our results show that preterm birth and RLN lesion have distinct yet pervasive effects on infant feeding. Altered feeding performance in these neurologically compromised infants may be due in part to changes in the activity of the palatopharyngeal arches. Support or Funding Information NIH R01HD088561
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