The Effects of Involuntary Respiratory Contractions on Cerebral Blood Flow during Maximal Apnoea in Trained Divers

Troy J Cross,Mihajlo Lojpur,Justin J Kavanagh,Zeljko Dujic,Petra Zubin Maslov,Toni Breskovic,Bruce D Johnson,Kelvin Kian Loong Wong

doi:10.1371/journal.pone.0066950

Abstract

The effects of involuntary respiratory contractions on the cerebral blood flow response to maximal apnoea is presently unclear. We hypothesised that while respiratory contractions may augment left ventricular stroke volume, cardiac output and ultimately cerebral blood flow during the struggle phase, these contractions would simultaneously cause marked ‘respiratory’ variability in blood flow to the brain. Respiratory, cardiovascular and cerebrovascular parameters were measured in ten trained, male apnoea divers during maximal ‘dry’ breath holding. Intrathoracic pressure was estimated via oesophageal pressure. Left ventricular stroke volume, cardiac output and mean arterial pressure were monitored using finger photoplethysmography, and cerebral blood flow velocity was obtained using transcranial ultrasound. The increasingly negative inspiratory intrathoracic pressure swings of the struggle phase significantly influenced the rise in left ventricular stroke volume (R 2 = 0.63, P<0.05), thereby contributing to the increase in cerebral blood flow velocity throughout this phase of apnoea. However, these contractions also caused marked respiratory variability in left ventricular stroke volume, cardiac output, mean arterial pressure and cerebral blood flow velocity during the struggle phase (R 2 = 0.99, P<0.05). Interestingly, the magnitude of respiratory variability in cerebral blood flow velocity was inversely correlated with struggle phase duration (R 2 = 0.71, P<0.05). This study confirms the hypothesis that, on the one hand, involuntary respiratory contractions facilitate cerebral haemodynamics during the struggle phase while, on the other, these contractions produce marked respiratory variability in blood flow to the brain. In addition, our findings indicate that such variability in cerebral blood flow negatively impacts on struggle phase duration, and thus impairs breath holding performance.

Highlights

A truly ‘maximal’ apnoea is typified by two distinct, temporal phases
The resting pulmonary function of our participants appeared within the normal range, where forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1) and FEV1/FVC were 6.5760.36 L (12065% predicted), 5.4060.25 L (11864% predicted) and 0.8260.01 (10061% predicted), respectively
The present study demonstrates that involuntary respiratory contractions significantly influence the rise in Cerebral blood flow velocity (CBFV) via facilitation of left ventricular stroke volume (LVSV) during the struggle phase of breath holding

Summary

Introduction

A truly ‘maximal’ apnoea is typified by two distinct, temporal phases. The first phase is a quiescent period where respiratory neuromuscular output is voluntarily suppressed, the glottis is closed, and no movement of the chest wall occurs (i.e., ‘easy-going’ phase) [1]. Several factors are known to influence the apnoea breakpoint, these factors include: the degree of hypoxaemia and hypercapnia; lung volume and rate of alveolar gas-exchange; and afferent information originating within the diaphragm during contraction [4,5,6,7]. In addition to these factors, the ability to maintain adequate delivery of O2 to the cerebral tissues must necessarily impact on breath holding performance [8,9], insofar as brain hypoxia/hypercapnia may induce cognitive impairment, unconsciousness and, in some cases, may result in fatality [10,11]. The question arises: What mechanisms exist to ensure an adequate supply of O2 to the cerebral tissues during maximal apnoea?

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