Effect of postnatal maturation on the mechanisms of esophageal propulsion in preterm human neonates: primary and secondary peristalsis

Abstract

Objectives: The changes in esophageal propulsive characteristics during maturation are not known. Our aim was to define the effects of postnatal maturation on esophageal peristaltic characteristics in preterm human neonates. We tested the hypotheses that: (i) maturation modifies esophageal bolus propulsion characteristics, and (ii) the mechanistic characteristics differ between primary and secondary peristalsis.

Methods: Esophageal motility in 10 premature neonates (mean 27.5 weeks gestational age) was evaluated twice at 33.8 weeks (time 1, earlier study) and 39.2 weeks (time 2, later study) mean postmenstrual age. Esophageal manometry waveform characteristics (amplitude and duration, peristaltic velocity, and intrabolus pressure domains) were analyzed during spontaneous primary peristalsis and infusion-induced secondary peristalsis. Repeated-measures and unstructured variance-covariance or compound symmetry matrixes were used for statistical comparison. Values stated as least squares means+/-s.e.m. or percent.

Results: A total of 200 primary peristalsis and 227 secondary peristalsis events were evaluated. Between time 1 and time 2: (i) proximal esophageal waveform amplitude increased (P<0.02), with primary peristalsis (38+/-6 vs. 48+/-7 mm Hg) and with secondary peristalsis (34+/-6 vs. 46+/-5 mm Hg); (ii) distal esophageal waveform amplitude was similar (P=NS), with primary peristalsis (42+/-4 vs. 43+/-4 mm Hg) and secondary peristalsis (29+/-3 vs. 32+/-4 mm Hg); (iii) proximal esophageal waveform onset to peak duration decreased (P=0.02) with primary (2.6+/-0.3 vs. 1.9+/-0.1 s, P<0.003) and with secondary peristalsis (2.2+/-0.2 vs. 1.8+/-0.1 s); (iv) distal esophageal waveform onset to peak duration decreased (P=0.01) with primary (2.4+/-0.3 vs. 1.8+/-0.1 s) and with secondary peristalsis (1.9+/-0.2 vs. 1.5+/-0.1 s); (v) effects of identical stimulus volume on intrabolus pressure were similar (P=NS); however, greater infusion volumes (2 vs. 1 ml) generated higher intrabolus pressure at both time 1 and time 2 (both Ps<0.05). Between primary and secondary peristalsis (mechanistic variable): (i) no differences were noted at either period, with proximal esophageal waveform amplitudes (P=NS); (ii) differences were noted with distal esophageal waveform amplitudes at each time period (P=0.0002); (iii) no differences were noted with both esophageal waveforms duration at either period (P=NS); (iv) peristaltic velocity was faster with secondary peristalsis than with primary peristalsis at either period (at earlier study, 7.9+/-1.4 vs. 2.5+/-1.4 cm/s and at later study 6.2+/-1.6 vs. 1.2+/-1.5 cm/s, both Ps<0.01).

Conclusions: In preterm neonates, longitudinal maturation modulates the characteristics of primary and secondary peristalsis. Differences in proximal striated muscle and distal smooth muscle activity during peristalsis are evident. Peristaltic velocity is faster with secondary peristalsis. These findings may represent maturation of central and peripheral neuromotor properties of esophageal bolus propulsion in healthy preterm human neonates.

Figure 1

Mechanisms of esophageal propulsion. (a) Waveform and contour plots of a primary peristalsis sequence. Note pharyngeal waveform, upper esophageal sphincter (UES) relaxation, and progression of primary peristalsis, and LES relaxation. Proximal (PE), middle (ME), and distal (DE) esophageal waveforms and contour plots are shown. Peak waveform amplitude, onset to peak duration, and peristaltic velocity were evaluated. The contour plot provides a two-dimensional color-coded visual representation of the same primary peristalsis sequence. (b) Waveform and contour plots of a secondary peristalsis sequence. Note the response to mid esophageal infusion (evidenced by common cavity and infusion signal) resulting in secondary peristalsis associated with LES relaxation. PE, ME, and DE esophageal waveforms and contour plots are shown. Note the absence of pharyngeal waveform and absence of UES relaxation that distinguishes secondary peristalsis. Peak waveform amplitude, onset to peak duration, and peristaltic velocity were evaluated. The contour plot provides a two-dimensional color-coded visual representation of the same secondary peristalsis sequence.

Figure 2

Maximum peristaltic waveform amplitude. In (a), the maturational changes in proximal esophageal segment showed significant increase with primary and secondary peristalsis (P < 0.02). In (b), the distal esophageal amplitude remained similar between time 1 and time 2 with both primary and secondary peristalsis. However, significant differences are noted between the mechanisms at both periods (P = 0.0002).

Figure 3

Duration of peristaltic waveform onset to peak. In proximal esophagus (a), decreasing trends with maturation during primary (P = 0.02) and during secondary peristalsis were visible. At either time points, there were no differences between the mechanisms. In distal esophagus (b), similar trends were noted with both primary and secondary peristalsis (both Ps = 0.01).

Figure 4

Peristaltic velocity between proximal to distal esophagus. Differences between the mechanisms (primary vs. secondary peristalsis) are evident at both the time points (both Ps < 0.01).

Figure 5

Intrabolus pressure. In (a), the relationship between infusion volume and intrabolus pressure is shown; higher volumes generated more intrabolus pressure at both periods (both Ps < 0.05). In (b), the relationship between infusion volume and the duration of exposure is shown. The duration of intrabolus pressure resulting in secondary peristalsis at time 2 was shorter (P < 0.05).

Figure 6

Overview of maturational and mechanistic effects on primary and secondary peristalsis.