Dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrations

Objectives: We aimed to quantify the magnitude and time transients of capillary blood flow responses to acute changes in local oxygen concentration ([O2]), and carbon dioxide concentration ([CO2]) in skeletal muscle. Additionally, we sought to quantify the combined response to both low [O2] and high...

Full description

Bibliographic Details
Main Authors: Gaylene M. Russell McEvoy, Brenda N. Wells, Meghan E. Kiley, Kanika K. Kaur, Graham M. Fraser
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2022.1052449/full
_version_ 1811212515361685504
author Gaylene M. Russell McEvoy
Brenda N. Wells
Meghan E. Kiley
Kanika K. Kaur
Graham M. Fraser
author_facet Gaylene M. Russell McEvoy
Brenda N. Wells
Meghan E. Kiley
Kanika K. Kaur
Graham M. Fraser
author_sort Gaylene M. Russell McEvoy
collection DOAJ
description Objectives: We aimed to quantify the magnitude and time transients of capillary blood flow responses to acute changes in local oxygen concentration ([O2]), and carbon dioxide concentration ([CO2]) in skeletal muscle. Additionally, we sought to quantify the combined response to both low [O2] and high [CO2] to mimic muscle microenvironment changes at the onset of exercise.Methods: 13 Sprague Dawley rats were anaesthetized, mechanically ventilated, and instrumented with indwelling catheters for systemic monitoring. The extensor digitorum longus muscle was blunt dissected, and reflected over a microfluidic gas exchange chamber in the stage of an inverted microscope. Four O2 challenges, four CO2 challenges, and a combined low O2 (7–2%) and high CO2 (5–10%) challenges were delivered to the surface with simultaneous visualization of capillary blood flow responses. Recordings were made for each challenge over a 1-min baseline period followed by a 2-min step change. The combined challenge employed a 1-min [O2] challenge followed by a 2-min change in [CO2]. Mean data for each sequence were fit using least-squared non-linear exponential models to determine the dynamics of each response.Results: 7–2% [O2] challenges decreased capillary RBC saturation within 2 s following the step change (46.53 ± 19.56% vs. 48.51 ± 19.02%, p < 0.0001, τ = 1.44 s), increased RBC velocity within 3 s (228.53 ± 190.39 μm/s vs. 235.74 ± 193.52 μm/s, p < 0.0003, τ = 35.54 s) with a 52% peak increase by the end of the challenge, hematocrit and supply rate show similar dynamics. 5–10% [CO2] challenges increased RBC velocity within 2 s following the step change (273.40 ± 218.06 μm/s vs. 276.75 ± 215.94 μm/s, p = 0.007, τ = 79.34s), with a 58% peak increase by the end of the challenge, supply rate and hematocrit show similar dynamics. Combined [O2] and [CO2] challenges resulted in additive responses to all microvascular hemodynamic measures with a 103% peak velocity increase by the end of the collection period. Data for mean responses and exponential fitting parameters are reported for all challenges.Conclusion: Microvascular level changes in muscle [O2] and [CO2] provoked capillary hemodynamic responses with differing time transients. Simulating exercise via combined [O2] and [CO2] challenges demonstrated the independent and additive nature of local blood flow responses to these agents.
first_indexed 2024-04-12T05:30:03Z
format Article
id doaj.art-524fb1553ba74fcf925669f366effdd6
institution Directory Open Access Journal
issn 1664-042X
language English
last_indexed 2024-04-12T05:30:03Z
publishDate 2022-12-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Physiology
spelling doaj.art-524fb1553ba74fcf925669f366effdd62022-12-22T03:46:06ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2022-12-011310.3389/fphys.2022.10524491052449Dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrationsGaylene M. Russell McEvoyBrenda N. WellsMeghan E. KileyKanika K. KaurGraham M. FraserObjectives: We aimed to quantify the magnitude and time transients of capillary blood flow responses to acute changes in local oxygen concentration ([O2]), and carbon dioxide concentration ([CO2]) in skeletal muscle. Additionally, we sought to quantify the combined response to both low [O2] and high [CO2] to mimic muscle microenvironment changes at the onset of exercise.Methods: 13 Sprague Dawley rats were anaesthetized, mechanically ventilated, and instrumented with indwelling catheters for systemic monitoring. The extensor digitorum longus muscle was blunt dissected, and reflected over a microfluidic gas exchange chamber in the stage of an inverted microscope. Four O2 challenges, four CO2 challenges, and a combined low O2 (7–2%) and high CO2 (5–10%) challenges were delivered to the surface with simultaneous visualization of capillary blood flow responses. Recordings were made for each challenge over a 1-min baseline period followed by a 2-min step change. The combined challenge employed a 1-min [O2] challenge followed by a 2-min change in [CO2]. Mean data for each sequence were fit using least-squared non-linear exponential models to determine the dynamics of each response.Results: 7–2% [O2] challenges decreased capillary RBC saturation within 2 s following the step change (46.53 ± 19.56% vs. 48.51 ± 19.02%, p < 0.0001, τ = 1.44 s), increased RBC velocity within 3 s (228.53 ± 190.39 μm/s vs. 235.74 ± 193.52 μm/s, p < 0.0003, τ = 35.54 s) with a 52% peak increase by the end of the challenge, hematocrit and supply rate show similar dynamics. 5–10% [CO2] challenges increased RBC velocity within 2 s following the step change (273.40 ± 218.06 μm/s vs. 276.75 ± 215.94 μm/s, p = 0.007, τ = 79.34s), with a 58% peak increase by the end of the challenge, supply rate and hematocrit show similar dynamics. Combined [O2] and [CO2] challenges resulted in additive responses to all microvascular hemodynamic measures with a 103% peak velocity increase by the end of the collection period. Data for mean responses and exponential fitting parameters are reported for all challenges.Conclusion: Microvascular level changes in muscle [O2] and [CO2] provoked capillary hemodynamic responses with differing time transients. Simulating exercise via combined [O2] and [CO2] challenges demonstrated the independent and additive nature of local blood flow responses to these agents.https://www.frontiersin.org/articles/10.3389/fphys.2022.1052449/fullmicrocirculationoxygen mediated blood flow regulationcapillaryskeletal muscleexercisecarbon dioxide
spellingShingle Gaylene M. Russell McEvoy
Brenda N. Wells
Meghan E. Kiley
Kanika K. Kaur
Graham M. Fraser
Dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrations
Frontiers in Physiology
microcirculation
oxygen mediated blood flow regulation
capillary
skeletal muscle
exercise
carbon dioxide
title Dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrations
title_full Dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrations
title_fullStr Dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrations
title_full_unstemmed Dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrations
title_short Dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrations
title_sort dynamics of capillary blood flow responses to acute local changes in oxygen and carbon dioxide concentrations
topic microcirculation
oxygen mediated blood flow regulation
capillary
skeletal muscle
exercise
carbon dioxide
url https://www.frontiersin.org/articles/10.3389/fphys.2022.1052449/full
work_keys_str_mv AT gaylenemrussellmcevoy dynamicsofcapillarybloodflowresponsestoacutelocalchangesinoxygenandcarbondioxideconcentrations
AT brendanwells dynamicsofcapillarybloodflowresponsestoacutelocalchangesinoxygenandcarbondioxideconcentrations
AT meghanekiley dynamicsofcapillarybloodflowresponsestoacutelocalchangesinoxygenandcarbondioxideconcentrations
AT kanikakkaur dynamicsofcapillarybloodflowresponsestoacutelocalchangesinoxygenandcarbondioxideconcentrations
AT grahammfraser dynamicsofcapillarybloodflowresponsestoacutelocalchangesinoxygenandcarbondioxideconcentrations