Biomechanical effects of esophageal elongation on the circumferential tension of the cervical esophagus in vivo

Abstract

Evidence obtained ex vivo suggests that physical elongation of the esophagus increases esophageal circumferential stress-strain ratio, but it is unknown whether this biomechanical effect alters esophageal function in vivo. We investigated the effects of physical or physiological elongation of the cervical esophagus on basal and active circumferential tension in vivo. The esophagus was elongated, using 29 decerebrate cats, either physically by distal physical extension of the esophagus or physiologically by stimulating the hypoglossal nerve, which activates laryngeal elevating muscles that elongate the esophagus. Hyoid, pharyngeal, and esophageal muscles were instrumented with electromyogram (EMG) electrodes and/or strain gauge force transducers. Esophageal intraluminal manometry was also recorded. We found that physical or physiological elongation of the cervical esophagus increased esophageal circumferential basal as well as active tension initiated by electrical stimulation of the pharyngo-esophageal nerve or the esophageal muscle directly, but did not increase esophageal intraluminal pressure or EMG activity. The esophageal circumferential response to the esophago-esophageal contractile reflex was increased by distal physical elongation, but not orad physiological elongation. We conclude that physical or physiological elongation of the esophagus significantly increases esophageal circumferential basal and active tension without muscle activation. We hypothesize that this effect is caused by an increase in esophageal stress-strain ratio by a biomechanical process, which increases circumferential wall stiffness. The increase in esophageal circumferential stiffness increases passive tension and the effectiveness of active tension. This increase in cervical esophageal circumferential stiffness may alter esophageal function.NEW & NOTEWORTHY Physical or physiological esophageal elongation increases esophageal circumferential active or passive tension by a biomechanical process, which causes a decrease in esophageal circumferential elasticity. This increased stiffness of the esophageal wall likely promotes esophageal bolus flow during various esophageal functions.

Keywords: circumferential wall tension; esophageal elongation; esophagus; stress-strain ratio.

Graphical abstract

Figure 1.

Effect of esophageal physical elongation on basal circumferential tension and reflex activated contraction of the esophagus. The figure shows that applying a force of 50 g (Eso Long Tension at the upward arrow) to pull the cervical esophagus distally increased the basal circumferential tension of the esophagus (E2 SG) about 5 g and increased the maximal response of the esophago-esophageal contractile reflex (EECR) at each distension volume. Note that the changes in E2 SG with increased (up arrow) or decreased (down arrow) esophageal elongation tension were not associated with changes in E2 EMG activity. Therefore, physical esophageal elongation increases both basal and active esophageal circumferential tension without a change in EMG. CP, cricopharyngeus; E#, esophagus number of centimeters from the CP; Eso Long, esophageal longitudinal; EMG, electromyography; g, gram; SG, strain gauge; Stim, EECR stimulation volume distension.

Figure 2.

Effect of esophageal physiological elongation on basal esophageal tension. This figure shows that stimulation of the hypoglossal nerve (HG) activates the geniohyoideus (GH) and increases circumferential tension of the esophagus (E2 SG). Contraction of the GH elevates the larynx and elongates the attached cervical esophagus. In addition, increasing stimulation parameters increased contractile strength of the GH and circumferential tension of the esophagus (E2 SG) proportionally. Therefore, physiological elongation of the esophagus increases basal esophageal circumferential tension. CP, cricopharyngeus; E#, esophagus number of centimeters from the CP; EMG, electromyography; g, gram; GH, geniohyoideus; Hz, Hertz; SG, strain gauge; TP, thyropharyngeus; V, volt.

Figure 3.

Lack of effect of physiological elongation of the esophagus on esophageal intraluminal pressure. This figure shows that stimulation of the HG, which contracted the GH and elevated the larynx and cervical esophagus and increased E2 SG tension, had no effect of esophageal intraluminal pressure at 2, 5, and 8 cm from the CP recorded by manometry. Therefore, physiological elongation of the esophagus which increases esophageal circumferential tension does not increase esophageal intraluminal pressure. E#, esophagus number of centimeters from the CP; EMG, electromyography; GH, geniohyoideus; HG Stim, hypoglossal nerve stimulation: g, gram; Hz, Hertz; Mano, manometry; SG, strain gauge; V, volt.

Figure 4.

Effect of esophageal physical elongation on esophageal circumferential tension ex vivo. This figure shows that after the esophagus was excised from the animal, pulling longitudinally on the esophagus caused an increase in esophageal circumferential tension. Note the strong correlation in magnitude and timing between the circumferential and longitudinal tensions. Therefore, the increase in circumferential tension caused by esophageal elongation is a function of the biomechanics of the tissue and not an active muscular response. The vertical arrow shows the short delay from stimulus, i.e., longitudinal tension, to response, i.e., circumferential tension. E#, esophagus number of centimeters from the cricopharyngeus; g, grams; SG, strain gauge.

Figure 5.

Quantitative effect of esophageal physical elongation on reflex activated contraction of the esophagus. This figure shows that elongation of the esophagus distally using a force from 50 to 100 g significantly increased the magnitude of the EECR responses of the cervical esophagus. Therefore, the effect of esophageal elongation on reflex contraction of the esophagus is statistically significant. *P < 0.05, n = 6. The horizontal bars are mean and SE. Ctl# or Exp#, control or experimental EECR response activated by number of milliliters stimulation. EECR, esophago-esophageal contractile reflex.

Figure 6.

Quantitative effect of esophageal physical elongation on reflex activated cervical esophageal EMG response. This graph shows that pulling distally on the cervical esophagus using a force from 50 to 100 g did not cause a statistically significant increase in EMG activity (P > 0.05, n = 5) caused by activation of the EECR. Therefore, esophageal elongation increases reflex activated contraction of the esophagus without any significant increase in activation of the esophageal striated muscle. The horizontal bars are mean and SE. # mL or # mL +, number of milliliters stimulation of EECR without (# mL) or with (# mL +) esophageal elongation. EECR, esophago-esophageal contractile reflex; EMG, electromyography.

Figure 7.

The effect of cervical esophageal physiological elongation on reflex activation of the esophagus. This figure shows that stimulation of the HG activates contraction of the GH, which elevates the larynx and elongates the esophagus and increases the magnitude of the esophageal circumferential tension, but not intraluminal pressure, at each volume of stimulation of the EECR. However, the increases in esophageal circumferential tension during simultaneous activation of EECR and HG stimulation are not greater than with EECR stimulation alone. Therefore, physiological elongation of the esophagus increases basal but not reflex activated circumferential esophageal tension. EECR, esophago-esophageal contractile reflex; E#, number of centimeters from the cricopharyngeus; EMG, electromyography; g, grams; GH, geniohyoideus; HG, hypoglossal nerve; Hz, Hertz; Mano, manometry; SG, strain gauge; Stim, stimulation; V, volt.

Figure 8.

Quantitation of the effect of physiological elongation of the esophagus on the reflex activation of esophageal circumferential tension. This graph shows that stimulation of the HG does not significantly [P > 0.05 (n = 5) for 1, 3, or 5 mL] increase the effects of EECR. The horizontal bars are mean and SE. Ctl# or Exp#, control or experimental EECR response activated by number of milliliters stimulation; HG, hypoglossal nerve.

Figure 9.

Effect of physical elongation of the cervical esophagus on the physiological activation of circumferential esophageal tension. This figure shows that applying distal forces of 50–100 g to the cervical esophagus increased the contractile response of the cervical esophagus to stimulation of the motor nerve of the cervical esophagus, i.e., the pharyngeal esophageal nerve (PEN). In addition, greater distal tension of about 100 g, i.e., the first increase in distal tension, had a greater effect than distal tension of about 50 g, i.e., the second increase in distal tension. CP, cricopharyngeus; E#, number of centimeters from the cricopharyngeus; EMG, electromyography; Eso Long Tension, longitudinal tension applied to the esophagus; g, grams; SG, strain gauge; TP, thyropharyngeus; V, volt.

Figure 10.

Effect of physiological elongation of the esophagus on the physiological activation of circumferential esophageal tension. This figure shows that stimulation of the HG increased the cervical esophageal circumferential response to stimulation of the PEN. The simultaneous stimulation of the PEN and HG increased (16.6 g) esophageal circumferential tension greater than the stimulation of PEN (9 g) and HG (2.5 g) individually. CP, cricopharyngeus; E#, number of centimeters from the CP; EMG, electromyography; g, grams; GH, geniohyoideus; HG, hypoglossal nerve; Hz, Hertz; PEN, pharyngo-esophageal nerve; SG, strain gauge; TP, thyropharyngeus; V, volt.

Figure 11.

Effect of physiological elongation of the esophagus on esophageal tension responses to direct stimulation of the esophagus. This figure shows that stimulation of the HG increased the esophageal circumferential response to direct electrical stimulation of the cervical esophageal muscle. That is, the simultaneous stimulation of HG and the esophagus directly (17.8 g) was greater than the addition of the HG (3.0 g) and esophagus (12.2 g) stimulated separately. CP, cricopharyngeus; E#, number of centimeters from the CP; Eso, esophagus; g, gram; HG, hypoglossal nerve; Hz, Hertz; TP, thyropharyngeus; V, volt.