Maturation of the Coordination Between Respiration and Deglutition with and Without Recurrent Laryngeal Nerve Lesion in an Animal Model

Abstract

The timing of the occurrence of a swallow in a respiratory cycle is critical for safe swallowing, and changes with infant development. Infants with damage to the recurrent laryngeal nerve, which receives sensory information from the larynx and supplies the intrinsic muscles of the larynx, experience a significant incidence of dysphagia. Using our validated infant pig model, we determined the interaction between this nerve damage and the coordination between respiration and swallowing during postnatal development. We recorded 23 infant pigs at two ages (neonatal and older, pre-weaning) feeding on milk with barium using simultaneous high-speed videofluoroscopy and measurements of thoracic movement. With a complete linear model, we tested for changes with maturation, and whether these changes are the same in control and lesioned individuals. We found (1) the timing of swallowing and respiration coordination changes with maturation; (2) no overall effect of RLN lesion on the timing of coordination, but (3) a greater magnitude of maturational change occurs with RLN injury. We also determined that animals with no surgical intervention did not differ from animals that had surgery for marker placement and a sham procedure for nerve lesion. The coordination between respiration and swallowing changes in normal, intact individuals to provide increased airway protection prior to weaning. Further, in animals with an RLN lesion, the maturation process has a larger effect. Finally, these results suggest a high level of brainstem sensorimotor interactions with respect to these two functions.

Keywords: Animal model; Deglutition; Development; Infant; Recurrent laryngeal nerve; Respiration; Sensorimotor.

Figure 1

Measurement of time of inspiration onset. The trace shows thoracic movement over time, with time = 0 set to the time milk transits over the laryngeal opening, the precise timing of the swallow. The amount of thoracic movement is idiosyncratic to the animal, depending on their size, and the values are scaled to maximum movement in the sequence. The lag from the swallow to the start of thoracic expansion was measured for each swallow in the data set.

Figure 2

Thoracic movement over a portion of a feeding sequence with swallows indicated by dotted lines. All data consisted of complete sequences of more than 50 swallows. 10–20 swallows per sequence were identified and selected from the XROMM visual data. The time equivalent data from the respiratory data were then extracted using the synchronization signal recorded on both data traces. In this example, neither respiration nor swallowing were regular.

Figure 3

Median thoracic movement and variation (interquartile range) for two sets of 20 swallows, representing two ages, aligned to the time of the swallow (time=0). The solid line is the median value at each time point of 20 respiratory cycles and the grey lines are the upper and lower quartiles from those cycles. The data were collected at 1kHz from the same animal. The value of thoracic movement is idiosyncratic to each animal. The value analyzed is the time of the start of inspiration after the swallow, indicated by the arrow on the x-axis.

Figure 4

Least square means showing the main effects and the interaction between treatment and age for the timing of inspiration. Error bars represent standard errors of LSM. The dotted line indicates the difference in response due to age within each treatment group. The significant interaction term indicates that this difference in the lesioned group is larger than the difference in the control group.