Breath-by-breath analysis of respiratory sinus arrhythmia in dogs
Introduction
The acceleration of the heart rhythm during the inspiratory phase of the breathing cycle, or Respiratory Sinus Arrhythmia (RSA), has long been recognised (Ludwig, 1847; brief historical overviews in Larsen et al., 2010 and Schaefer et al., 2014). Although usually detected by electrocardiography, in some humans RSA can be revealed at auscultation of the heart or palpation of the peripheral pulse. The inspiratory acceleration results from the transient inhibition of the cardiac vagal motoneurons of the nucleus ambiguus, which constitutes the cardio-inhibitory center (Farmer et al., 2016). During inspiration, central and peripheral stimuli inhibit the parasympathetic output, tilting the balance in favor of the sympathetic arm of the control of heart rate (HR). The inspiration-related peripheral stimuli include activation of airway stretch receptors, the rise in venous return (or ‘Bainbridge reflex’) and the stimulation of the cardiac vasopressors. Probably more important are the central inputs on the nucleus ambiguous from the centers of respiratory rhythmogenesis (Daly, 1986). Because of the inhibition of the vagal control, the magnitude of RSA is often considered an indicator of ‘vagal tone’ for a variety of body functions, and its changes have been used as predictors of patient’s outcome for cardiac diseases and other disorders (e.g., Schechtman et al., 1992; Fei et al., 1996a, 1996b; La Rovere et al., 2003; Tonhajzerova et al., 2009).
Althouh power spectrum analysis can detect RSA (Malik, 1996; Barnett et al., 1999), a precise quantification of the RSA magnitude requires the synchronous measures of pneumogram and beat-by-beat instantanelous heart rate (hR); hence, for each breath, RSA is the difference between the highest inspiratory hR-peak and the lowest expiratory hR-trough. The breath-by breath approach has been applied mostly to humans (Hirsch and Bishop, 1981; Taha et al., 1995; Mortola et al., 2015, 2016, 2020) and occasionaly to other species (Hanton and Rabemampianina, 2006; Piccione et al., 2019). By expressing the peak-trough difference in hR in percent of the mean HR, it is possible to compare RSA among individuals or species. By such approach, in humans, RSA averaged about 12 % of mean HR (Mortola et al., 2018), and in four horses it was 9% (Piccione et al., 2019); in both species the variability among subjects was large. In humans, voluntary changes in breathing pattern modify RSA; for example faster and shallower breathing decreases RSA (Hirsch and Bishop, 1981). Differently, changes in HR with muscle exercise under voluntary control of breathing have lesser effects (Mortola et al., 2018). Whether a correlation exists between RSA and HR or breathing rate (BR) among individuals at rest is still unknown. Dogs offer an opportunity to investigate putative correlations because of their large variation in body weight, unparalleled among mammals, with large ranges in HR and BR. Furthermore, in dogs just a few months old (Haddad et al., 1984; Bernal et al., 1995), the electrocardiogram often indicated the presence of a pronounced sinus arrhythmia attributable to breathing (e.g., Hayano et al., 1996), which facilitates the analysis and reduces the possibility of errors.
The present study aimed to evaluate the correlation between RSA and HR, BR and IBI variability in resting dogs of different body sizes. In addition, the breath-by-breath analysis allowed to consider the relationship between RSA and hR-peaks and hR-troughs; this latter reflects the balance between vagal and sympathgetic control of HR in absence of respiratory interference. Finally, in two dogs with frequent panting episodes, analysis of the transition from resting breathing to panting has unvailed the importance of central factors in the origin of RSA.
Section snippets
Methods
The experiments were conducted with the approval of the Ethic Committee of the University of Pisa (OPBA #49/2019). Almost all measurements were obtained in the am hours (9:00−12:00) from 25 dogs of different breeds. Two of these dogs were panting (breathing frequency more than twice the average) for most of the recording time; their data were considered separately from those of the main group. In these dogs, panting probably reflected the emotional response to the lab environment (Bragg et al.,
Results
Table 2 summarizes the average resting values for each dog. In many dogs even a cursory look at the ECG recording indicated obvious changes of the IBI (and of its reciprocal hR) in phase with breathing (Fig. 1, Fig. 2).
RSA averaged 40.1 % ±4.5, with large inter-individual variations, from 9 to 85 % (Table 2). The smaller the RSA, the larger its breath-by-breath variability (r = 0.62, P < 0.01; Fig. 3). The average RSA value of the four males (42.3 ± 12.2 %) did not differ significantly from the
Discussion
A common approach to analyze a sequence of events like the IBI series is by frequency domain analysis, whereby the series is analyzed for its frequency content. Then, the frequency range of the IBI spectrum that corresponds to BR is attributed to RSA (Malik, 1996; Barnett et al., 1999). In dogs, spectrum analysis of IBI to identify RSA has been performed often (Haddad et al., 1984; Minors and O’Grady, 1997; Olsen et al., 1999; Yasuma and Hayano, 2001; Yasuma et al., 2001), although the
Acknowledgements
We like to thank Francesca Bonelli and Micaela Sgorbini for their contribution and interest in the early phase of study planning.
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