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Effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing
Background: Periodic breathing (PB) is a cyclical breathing pattern composed of alternating periods of hyperventilation (hyperpnea, HP) and central apnea (CA). Differences in PB phenotypes mainly reside in HP length. Given that respiration modulates muscle sympathetic nerve activity (MSNA), which de...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9483206/ https://www.ncbi.nlm.nih.gov/pubmed/36134331 http://dx.doi.org/10.3389/fphys.2022.934372 |
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author | Spiesshoefer, Jens Giannoni, Alberto Borrelli, Chiara Sciarrone, Paolo Husstedt, Imke Emdin, Michele Passino, Claudio Kahles, Florian Dawood, Tye Regmi, Binaya Naughton, Matthew Dreher, Michael Boentert, Matthias Macefield, Vaughan G. |
author_facet | Spiesshoefer, Jens Giannoni, Alberto Borrelli, Chiara Sciarrone, Paolo Husstedt, Imke Emdin, Michele Passino, Claudio Kahles, Florian Dawood, Tye Regmi, Binaya Naughton, Matthew Dreher, Michael Boentert, Matthias Macefield, Vaughan G. |
author_sort | Spiesshoefer, Jens |
collection | PubMed |
description | Background: Periodic breathing (PB) is a cyclical breathing pattern composed of alternating periods of hyperventilation (hyperpnea, HP) and central apnea (CA). Differences in PB phenotypes mainly reside in HP length. Given that respiration modulates muscle sympathetic nerve activity (MSNA), which decreases during HP and increases during CA, the net effects of PB on MSNA may critically depend on HP length. Objectives: We hypothesized that PB with shorter periods of HP is associated with increased MSNA and decreased heart rate variability. Methods: 10 healthy participants underwent microelectrode recordings of MSNA from the common peroneal nerve along with non-invasive recording of HRV, blood pressure and respiration. Following a 10-min period of tidal breathing, participants were asked to simulate PB for 3 min following a computed respiratory waveform that emulated two PB patterns, comprising a constant CA of 20 s duration and HP of two different lengths: short (20 s) vs long (40 s). Results: Compared to (3 min of) normal breathing, simulated PB with short HP resulted in a marked increase in mean and maximum MSNA amplitude (from 3.2 ± 0.8 to 3.4 ± 0.8 µV, p = 0.04; from 3.8 ± 0.9 to 4.3 ± 1.1 µV, p = 0.04, respectively). This was paralleled by an increase in LF/HF ratio of heart rate variability (from 0.9 ± 0.5 to 2.0 ± 1.3; p = 0.04). In contrast, MSNA response to simulated PB with long HP did not change as compared to normal breathing. Single CA events consistently resulted in markedly increased MSNA (all p < 0.01) when compared to the preceding HPs, while periods of HP, regardless of duration, decreased MSNA (p < 0.05) when compared to normal breathing. Conclusion: Overall, the net effects of PB in healthy subjects over time on MSNA are dependent on the relative duration of HP: increased sympathetic outflow is seen during PB with a short but not with a long period of HP. |
format | Online Article Text |
id | pubmed-9483206 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-94832062022-09-20 Effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing Spiesshoefer, Jens Giannoni, Alberto Borrelli, Chiara Sciarrone, Paolo Husstedt, Imke Emdin, Michele Passino, Claudio Kahles, Florian Dawood, Tye Regmi, Binaya Naughton, Matthew Dreher, Michael Boentert, Matthias Macefield, Vaughan G. Front Physiol Physiology Background: Periodic breathing (PB) is a cyclical breathing pattern composed of alternating periods of hyperventilation (hyperpnea, HP) and central apnea (CA). Differences in PB phenotypes mainly reside in HP length. Given that respiration modulates muscle sympathetic nerve activity (MSNA), which decreases during HP and increases during CA, the net effects of PB on MSNA may critically depend on HP length. Objectives: We hypothesized that PB with shorter periods of HP is associated with increased MSNA and decreased heart rate variability. Methods: 10 healthy participants underwent microelectrode recordings of MSNA from the common peroneal nerve along with non-invasive recording of HRV, blood pressure and respiration. Following a 10-min period of tidal breathing, participants were asked to simulate PB for 3 min following a computed respiratory waveform that emulated two PB patterns, comprising a constant CA of 20 s duration and HP of two different lengths: short (20 s) vs long (40 s). Results: Compared to (3 min of) normal breathing, simulated PB with short HP resulted in a marked increase in mean and maximum MSNA amplitude (from 3.2 ± 0.8 to 3.4 ± 0.8 µV, p = 0.04; from 3.8 ± 0.9 to 4.3 ± 1.1 µV, p = 0.04, respectively). This was paralleled by an increase in LF/HF ratio of heart rate variability (from 0.9 ± 0.5 to 2.0 ± 1.3; p = 0.04). In contrast, MSNA response to simulated PB with long HP did not change as compared to normal breathing. Single CA events consistently resulted in markedly increased MSNA (all p < 0.01) when compared to the preceding HPs, while periods of HP, regardless of duration, decreased MSNA (p < 0.05) when compared to normal breathing. Conclusion: Overall, the net effects of PB in healthy subjects over time on MSNA are dependent on the relative duration of HP: increased sympathetic outflow is seen during PB with a short but not with a long period of HP. Frontiers Media S.A. 2022-09-05 /pmc/articles/PMC9483206/ /pubmed/36134331 http://dx.doi.org/10.3389/fphys.2022.934372 Text en Copyright © 2022 Spiesshoefer, Giannoni, Borrelli, Sciarrone, Husstedt, Emdin, Passino, Kahles, Dawood, Regmi, Naughton, Dreher, Boentert and Macefield. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Physiology Spiesshoefer, Jens Giannoni, Alberto Borrelli, Chiara Sciarrone, Paolo Husstedt, Imke Emdin, Michele Passino, Claudio Kahles, Florian Dawood, Tye Regmi, Binaya Naughton, Matthew Dreher, Michael Boentert, Matthias Macefield, Vaughan G. Effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing |
title | Effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing |
title_full | Effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing |
title_fullStr | Effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing |
title_full_unstemmed | Effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing |
title_short | Effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing |
title_sort | effects of hyperventilation length on muscle sympathetic nerve activity in healthy humans simulating periodic breathing |
topic | Physiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9483206/ https://www.ncbi.nlm.nih.gov/pubmed/36134331 http://dx.doi.org/10.3389/fphys.2022.934372 |
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