Elsevier

Physiology & Behavior

Volume 142, 1 April 2015, Pages 52-56
Physiology & Behavior

Coordination of oro-pharyngeal food transport during chewing and respiratory phase

https://doi.org/10.1016/j.physbeh.2015.01.035Get rights and content

Highlights

  • Onset of Stage II transport and swallowing cycles was predominantly during expiration.

  • Onset of chewing cycles was comparatively less often during expiration.

  • Neural control of respiratory phase varies among these three feeding behaviors.

  • Expiratory airflow during stage II transport may reduce prandial aspiration.

Abstract

When eating solid food, the tongue intermittently propels triturated food to the oropharynx or valleculae, where a bolus accumulates before swallowing. The tongue motion during this food transport (stage II transport, STII) is distinctly different from that during chewing, and is more similar to the oral propulsive stage of swallowing. Therefore, we tested the hypothesis that the onset of STII cycles was more likely to occur during expiration than inspiration. Videofluorography was recorded in a lateral projection while 10 healthy subjects ate solid foods. Respiration was concurrently monitored with plethysmography. Jaw motion cycles were classified as masticatory or swallowing. Masticatory cycles were further divided into chewing cycles and STII cycles. STII cycles were defined as those with bolus propulsion through the fauces by the tongue squeezing against the palate (without swallowing). Overall, 28% (62/223) of chewing cycles were initiated during inspiration, compared with only 12% (9/76) of STII cycles in this phase. The fraction of masticatory cycles occurring during inspiration was significantly smaller for STII cycles than for chewing cycles (Odds Ratio: 0.37 [95% CI: 0.17–0.78], p = 0.01). All 36 swallowing cycles had onset during expiration. Our findings reveal that stage II oro-pharyngeal food transport is linked to expiration, as is the oral propulsive stage of swallowing. This suggests a similarity in the neural control of these two feeding behaviors.

Introduction

The pharynx is a common passage for breathing and eating but is used in different ways. The pharynx is dilated to maintain airway patency for breathing, but for swallowing, the pharynx is constricted to push the food bolus propelled from the oral cavity to the esophagus. Respiratory phases surrounding swallowing are well controlled by the central nervous system to prevent inhalation of food and drink during swallowing; indeed, there is a pause in breathing during the swallow. A number of studies, using various measurement systems and different food consistencies, confirm that onset of swallowing is usually during expiration and breathing resumes in expiration after swallowing. Thus, the predominant respiration–swallowing pattern for a single liquid bolus swallow in adult humans is “exhale–swallow–exhale” (67–79% of liquid swallows), followed by “inhale–swallow–exhale” (18–21%) [1], [2], [3]. When eating solid food, swallowing is predominantly initiated during expiration (87–99%) [4], [5], [6].

Except for crucial moments surrounding the swallow, mastication and respiration have an inconsistent temporal relationship. When eating solid food, the tongue squeezes triturated food back along the palate to the oropharynx or valleculae, where a bolus is formed for up to 10 s before onset of swallowing. The food accumulating in the oropharynx is located in the path of respiratory airflow during mastication; this could potentially increase the risk of aspiration. Indeed, air can be inhaled through the pharyngeal airway while food is but a few millimeters above the laryngeal aditus. However, our previous study revealed that there is no consistent phase of respiration during the period of bolus aggregation in the pharynx [5]. There can be inspiration, expiration, or a pause in breathing during bolus aggregation, and in some cases there are multiple respiratory cycles during a single period of bolus aggregation in the pharynx.

The transport of a bolus of chewed and softened food from the oral cavity to the oropharynx during chewing is called stage II transport (STII) [7]. The tongue motion of STII is similar to the motion for the oral propulsive stage of swallowing and quite different than that for chewing. For chewing, the tongue shifts and rotates toward to the working side of the jaw to place the food on the occlusal surface of the lower teeth, but in STII, the tongue surface moves directly upward to contact the palate beginning with the anterior tongue and progressing posteriorly [8], [9] much as it does for the oral propulsive stage of the swallow. For liquid swallowing, oro-pharyngeal bolus transport is thought to be a part of a consecutive swallowing process that is regulated by the medullary swallowing center. Swallowing is usually initiated during expiration both when drinking a liquid bolus and when eating solid food [4], [5], [10]. The relationship between stage II transport and phase of respiration has not been reported. In the present study, we tested the hypothesis that stage II transport is more frequent during expiration than inspiration while feeding on solid food.

Section snippets

Data acquisition

The study protocol was approved by the Institutional Review Board (Application No. 86-06-25-03). Ten healthy, asymptomatic young adults (6 men, 4 women, median age: 25 yrs., range: 18–39 yrs.) participated after giving written informed consent. Dental occlusion was Class I in all subjects. Subjects were seated comfortably in a chair and ate 6 g each of banana and shortbread cookie lightly coated with barium powder while videofluorography (VFG) at 30 fps was recorded on a digital-video (DV) tape

Results

We collected a total of 335 jaw motion cycles, including 299 masticatory cycles and 36 swallowing cycles, from our 10 subjects. Of the 299 masticatory cycles, there were 223 chewing cycles and 76 STII cycles. STII cycles were interspersed among chewing cycles at a frequency that increased as the feeding sequence progressed toward a swallow (Fig. 2).

The percentage of cycles initiated during inspiration ranged among subjects from 17% (3/18 jaw cycles) to 41% (7/17) for chewing cycles and from 0%

Discussion

We found that stage II transport cycles were initiated significantly less frequently during inspiration (and thus, more frequently during expiration) in comparison to chewing cycles. Although feeding is a sequential process whose cycles may be affected by the one prior, our analysis of jaw motion cycles immediately following a STII cycle showed a similar trend (albeit not statistically significant) toward STII cycle initiation during expiration. Even consecutive STII cycles showed a tendency

Acknowledgments

The late Dr. Karen Hiiemae contributed immeasurably to the planning and design of this study. Chune Yang provided superb technical assistance. This research was supported by USPHS Award R01 DC 02123 from the National Institute on Deafness and other Communication Disorders and a Grant-in-Aid for Scientific Research (21792163, 26463200) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

The authors declare that there are no conflicts of interest.

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