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...
Main Authors: | , , , , |
---|---|
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 |