Non-nutritive swallowing and respiration coordination in full-term newborn lambs

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Abstract

Swallowing is a powerful inhibitor of respiratory rhythm in infants. The present study was aimed at investigating the influence of states of alertness on non-nutritive swallowing (NNS) frequency, on NNS and respiration coordination, and on bursts of NNS frequency in newborn lambs. Six full term newborn lambs were instrumented for electroencephalogram, eye movement, diaphragm and thyroarytenoid muscle electromyogram, nasal flow and electrocardiogram. Polysomnographic recordings were performed in non-sedated lambs, using radiotelemetry. NNS frequency was significantly higher during quiet wakefulness (W) and active sleep (AS) than during quiet sleep (QS). NNS mainly interrupted inspiration and the transition phases between expiration and inspiration, especially in W and AS. Bursts of NNS occurred significantly more often during AS. This study highlights the relevance of the ovine model to study ontogeny of NNS during sleep, and documents the influence of sleep on NNS and respiration coordination.

Introduction

The pharynx is involved in a number of functions including feeding and respiration. Swallowing activity has been consistently associated with brief respiratory inhibition in adults (Nishino et al., 1985, Preiksaitis et al., 1992, Shaker et al., 1992, McFarland and Lund, 1995, Paydarfar et al., 1995, Hiss et al., 2001). In newborns with central neural immaturity, there is a potential for respiratory compromise due to problems in coordinating both of these functions. Indeed, repetitive nutritive swallowing activity in newborns has been reported to disrupt respiratory rhythm with either respiratory inhibition (central apnea/hypopnea) or persistence of inspiratory efforts against upper airway closure (obstructive apneas) (Wilson et al., 1981, Koenig et al., 1990, Bamford et al., 1992). Similarly, non-nutritive swallowing (NNS) has been associated with both central and obstructive apneas in the newborn (Belgaumkar and Scott, 1976, Menon et al., 1984, Roberts et al., 1985, Thach and Menon, 1985, Miller and DiFiore, 1995). Although these observations have certainly underlined the clinical relevance of studying NNS in furthering our understanding of the pathophysiology of neonatal apneas, our knowledge of NNS in newborns is far from complete. Only one recent study has assessed the effects of state of alertness on NNS frequency in full term and preterm infants (Jeffery et al., 2000). Moreover, while several studies in neonates have examined the modification of respiratory function during nutritive swallowing (Thach and Menon, 1985, Koenig et al., 1990, Bamford et al., 1992, German et al., 1998), there is only one report assessing the coordination of NNS and respiration in infants (Wilson et al., 1981). Moreover, the effects of sleep state on this coordination have never been reported. Finally, we have previously observed bursts of NNS impeding ventilation during AS (Kianicka and Praud, 1997). Hence, the aim of the present study in newborn lambs was to examine the effects of state of alertness: (1) on NNS frequency, testing the hypothesis that NNS frequency is significantly higher in wakefulness (W) and active sleep (AS) than in quiet sleep (QS); (2) on coordination between NNS and respiratory cycle, testing the hypothesis that NNS can occur during all three phases of the respiratory cycle in all three states of alertness; and (3) on the occurrence of bursts of NNS, testing the hypothesis that bursts of NNS occur mainly in AS. Concomitantly, we also aimed to determine whether the newborn lamb (1st week after birth) is a valid animal model for studying NNS. This would pave the way for various studies on the relationships between NNS and neonatal respiration, including the effects of preterm birth using our recently developed preterm ovine model (Renolleau et al., 1999).

Section snippets

Animals

Six lambs were involved in the study. All lambs were born at term by spontaneous vaginal delivery and housed with their mothers in our animal quarters. The study protocol was approved by the ethics committee of the University of Sherbrooke for animal care and experimentation.

Surgical preparation

Surgery was performed 1–2 days after birth under general anesthesia (Ethane 1–2%+N2O 30%+O2 68%). Atropine sulfate (150 μg kg−1 subcutaneously) was given preoperatively with ketamine 10 mg kg−1 (Ketalean, Bimeda-MTC,

NNS activity frequency

Duration of states of alertness was 85±45 min (range 42–162) for W, 70±10 min (range 60–88) for QS, and 18±10 min (5–31) for AS. Active and quiet W duration were, respectively 60±37 (range 16–119) and 25±10 min (13–42). A total of 698 NNS was observed (312 in quiet W, 219 in QS and 167 in AS). NNS frequency (excluding burst of NNS) was significantly higher in quiet W [121±9 h−1 (range 112–132)] (P<0.0001) and AS [85±38 h−1 (range 43–150)] (P=0.0024) than during QS [31±13 h−1 (range 14–38)] (

Discussion

The present study extends previous knowledge and provides new data on the effects of states of alertness on coordination between respiration and NNS in newborn lambs. Our results show: (1) that NNS are more frequent in W and AS than in QS; (2) that NNS occur mainly during inspiration, and at the transition phases between expiration and inspiration; and (3) that NNS bursts occur mainly during AS, and can be associated with obstructive apnea.

Conclusion

Our results on the NNS activity in newborn lambs bear many similarities to observations in human newborns, including higher occurrence in AS and induction of apneas by bursts of NNS. Thus, the newborn lamb appears as a useful model for investigating the ontogeny of the coordination between respiration and NNS during various states of alertness. Such investigations include diverse situations such as hypoxia, or the use of medication (e.g. xanthines) or CPAP treatment, in full- and preterm lambs.

Acknowledgements

The authors thank Bruno Gagné and Christophe Grenier for their technical assistance, and Robert Brouillette for the critical review of the manuscript. Philippe Reix is a scholar of the Société de pneumologie de langue française. Jean-Paul Praud is a senior scholar of the Fonds de la recherche en santé du Québec. The research was supported by the Canadian Institutes of Health Research (grant MT15558), and the Fonds de la recherche en santé du Québec.

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