Development of the movement of the epiglottis in infant and juvenile pigs

Abstract

Although backward folding of the epiglottis is one of the signal events of the mammalian adult swallow, the epiglottis does not fold during the infant swallow. How this functional change occurs is unknown, but we hypothesize that a change in swallow mechanism occurs with maturation, prior to weaning. Using videofluoroscopy, we found three characteristic patterns of swallowing movement at different ages in the pig: an infant swallow, a transitional swallow and a post-weaning (juvenile or adult) swallow. In animals of all ages, the dorsal region of the epiglottis and larynx was held in an intranarial position by a muscular sphincter formed by the palatopharyngeal arch. In the infant swallow, increasing pressure in the oropharynx forced a liquid bolus through the piriform recesses on either side of a relatively stationary epiglottis into the esophagus. As the infant matured, the palatopharyngeal arch and the soft palate elevated at the beginning of the swallow, so exposing a larger area of the epiglottis to bolus pressure. In transitional swallows, the epiglottis was tilted backward relatively slowly by a combination of bolus pressure and squeezing of the epiglottis by closure of the palatopharyngeal sphincter. The bolus, however, traveled alongside but never over the tip of the epiglottis. In the juvenile swallow, the bolus always passed over the tip of the epiglottis. The tilting of the epiglottis resulted from several factors, including the action of the palatopharyngeal sphincter, higher bolus pressure exerted on the epiglottis and the allometry of increased size. In both transitional and juvenile swallows, the subsequent relaxation of the palatopharyngeal sphincter released the epiglottis, which sprang back to its original intranarial position.

Fig. 1

Schematic sagittal section through the head of a juvenile pig to aid in the interpretation of the video frames included in figure 2, figure 3, figure 4 and figure 7. See Results for description of this figure.

Fig. 2

(A) Photograph of a mid-line sagittal section through the larynx and posterior oral region. (B) Key to the structures in A. The dotted line indicates the palatopharyngeal muscle that runs lateral to the epiglottis from the anterior part of the soft palate to the roof of the hypopharynx.

Fig. 3

Photograph from a dorsal perspective. The palatopharyngeus sphincter has been cut open, and the passageway through the pharynx into the esophagus is visible. When intact, this muscle grips the laryngeal cartilages.

Fig. 4

(A–D) Infant swallow. Tracings from radiographs of a swallow (during suckling from a bottle) in which the milk is forced by tongue pressure to flow back laterally to the larynx via the piriform recess, to the hypopharynx. The larynx was in an intranarial position with the epiglottis lying above the anterior part of the soft palate. The patent airway was visible. Each tracing was obtained at the intervals shown in milliseconds after the onset of the swallow; these are based on recording at 29.97 frames per second, so that each videographic frame took approximately 33 ms. (E) Orbit of movement of a marker on the tip of the epiglottis during a single swallow. The teardrop shape of the marker indicates the orientation of the epiglottal tip (thick part of marker was anterior at rest). Abbrev.: asp = anterior part of soft palate; epm = marker in the tip of epiglottis; hp = hypopharynx; op = oropharynx; pa = patent airway; php = plane of the hard palate; pi = piriform recess; to = tongue.

Fig. 5

Transitional swallow. Milk suckled from a bottle reaches the hypopharynx and esophagus via both the piriform recesses and by traveling on either side of a flexed epiglottis (A and B). Dotted lines indicate the position of the palatopharyngeal arch (ppa) and radio-opaque markers within the arch (pp1 and pp2). The tip of the epiglottis lies above the palatophayngeal arch in A and B and only flips below the palatopharyngeal sphincter when the most flexed position is reached (C). The flexed epiglottis is initially drawn forward below the palatopharyngeal arch (D), and flips forward (arrow) when the sphincter relaxes (E). Abbrev.: asp = anterior part of soft palate; ep = epiglottis; es = esophagus; fa = faucial opening; hp = hypopharynx; np = nasopharynx; op = oropharynx; pa = patent airway; php = plane of the hard palate; pi = piriform recess; pp1 = anterior marker in palatopharyngeal arch; pp2 = posterior marker in palatopharyngeal arch; ppa = palatopharyngeal arch; t = trachea; thm = marker in antero-ventral region of the thyroid cartilage; to = tongue.

Fig. 6

Transitional swallow. Orbits of movement of markers in the tip of the epiglottis (epm), anterior part of the palatopharyngeal arch (pp1) and base of the thyroid cartilage (thm) as seen in lateral (A) and dorso-ventral (B) view. The orbit of movement of the thyroid marker is shown only in A. Plane of the hard palate (php) is indicated as a horizontal line.

Fig. 7

Dorsoventral view of five stages (A–E) during a transitional swallow. Many structures could not be clearly visualized in this view. A marker on the tip of the epiglottis (epm) is indicated by a black arrowhead anterior to a wide open glottis and trachea. At the beginning of the swallow (A), milk, shaded in grey, was visible against the anterior surface of the epiglottis and extended into the piriform recess. As the swallow commenced (B), milk was forced into the hypopharynx around the open glottis, obscuring the view of structures previously visible. In (C), the epiglottis was tilted backward, but its tip still pointed forward. Milk covered the entire surface of the epiglottis except the tip, which (from lateral view data) was still above the palatopharyngeal sphincter. The glottis was no longer visible and was presumably closed. In (D), milk had been cleared from the hypopharynx, the tip of the epiglottis pointed backward and (from lateral view data) was positioned below the closed palatopharyngeal sphincter. In E, the epiglottis had returned to an intranarial position and the glottis was open. Abbrev.: ep = epiglottis; es = esophagus; gl = glottis; hp = hypopharynx; pi = piriform recess; t = trachea.

Fig. 8

Juvenile swallow. Tracings are taken from radiographs of a swallow in a juvenile pig during drinking from a bowl (A). Bolus movement was associated with displacement of the epiglottis to an upright position (B). The epiglottis flexed rapidly below the palatopharyngeal sphincter as the milk passed over the downturned epiglottis (C, D) and then returned to its resting position (E). The orbit of movement of the epiglottal marker during the swallow is shown in (F). The scale for (A–E) is shown in the upper right corner, the scale for (F) directly below the figure. Note that the orientation of the head (plane of the hard palate, php) differs from that shown in figure 4 and figure 5 where the head was horizontal during suckling from a bottle. The head was tilted down at approximately 45° from the horizontal while drinking from a bowl. Abbrev.: asp = anterior part of soft palate; ep = epiglottis; op = oropharynx; pa = patent airway; pi = piriform recess; ppa = palatopharyngeal arch.