Studies into the determinants of skeletal muscle oxygen consumption: novel insight from near‐infrared diffuse correlation spectroscopy

Abstract

Key points Diffuse correlation spectroscopy (DCS) is emerging as a powerful tool to assess skeletal muscle perfusion. Near‐infrared spectroscopy (NIRS) is an established technique for characterizing the transport and utilization of oxygen through the microcirculation. Here we compared a combined NIRS–DCS system with conventional measures of oxygen delivery and utilization during handgrip exercise. The data show good concurrent validity between convective oxygen delivery and DCS‐derived blood flow index, as well as between oxygen extraction at the conduit and microvascular level. We then manipulated forearm arterial perfusion pressure by adjusting the position of the exercising arm relative to the position of the heart. The data show that microvascular perfusion can be uncoupled from convective oxygen delivery, and that tissue saturation seemingly compensates to maintain skeletal muscle oxygen consumption. Taken together, these data support a novel role for NIRS–DCS in understanding the determinants of muscle oxygen consumption at the microvascular level. Abstract Diffuse correlation spectroscopy (DCS) is emerging as a powerful tool to assess skeletal muscle perfusion. Combining DCS with near‐infrared spectroscopy (NIRS) introduces exciting possibilities for understanding the determinants of muscle oxygen consumption; however, no investigation has directly compared NIRS–DCS to conventional measures of oxygen delivery and utilization in an exercising limb. To address this knowledge gap, nine healthy males performed rhythmic handgrip exercise with simultaneous measurements by NIRS–DCS, Doppler blood flow and venous oxygen content. The two approaches showed good concurrent validity, with directionally similar responses between: (a) Doppler‐derived forearm blood flow and DCS‐derived blood flow index (BFI), and (b) venous oxygen saturation and NIRS‐derived tissue saturation. To explore the utility of combined NIRS–DCS across the physiological spectrum, we manipulated forearm arterial perfusion pressure by altering the arm position above or below the level of the heart. As expected, Doppler‐derived skeletal muscle blood flow increased with exercise in both arm positions, but with markedly different magnitudes (below: +424.3 ± 41.4 ml/min, above: +306 ± 12.0 ml/min, P = 0.002). In contrast, DCS‐derived microvascular BFI increased to a similar extent with exercise, regardless of arm position (P = 0.65). Importantly, however, the time to reach BFI steady state was markedly slower with the arm above the heart, supporting the experimental design. Notably, we observed faster tissue desaturation at the onset of exercise with the arm above the heart, resulting in similar muscle oxygen consumption profiles throughout exercise. Taken together, these data support a novel role for NIRS–DCS in understanding the determinants of skeletal muscle oxygen utilization non‐invasively and throughout exercise.

Near-infrared diffuse correlation spectroscopy tracks changes in oxygen delivery and utilization during exercise with and without isolated arterial compression

“…Near-infrared diffuse correlation spectroscopy. The methodology and validation of our in-house, dual-wavelength DCS system has previously been published (3,39,46). The system consists of two continuous-wave, long-coherence-length laser diodes (785 nm and 852 nm; Crystalaser, Reno, NV) that are alternatively switched (MEMS 2ϫ2 Blocking Switch, Dicon Fiberoptics, Richmond, CA) and a single-photon-counting avalanche photodiode (APD) as the photon detector (SPCM-AQRH-14-FC, Pacer USA, Palm Beach Gardens, FL).…”

“…Diffuse correlation spectroscopy (DCS) is an emerging optical imaging approach to measure skeletal muscle perfusion during exercise (3,22,39,46). DCS is completely noninvasive and has high temporal resolution for measuring relative changes in blood flow at the level of the microvasculature (3,7).…”

“…Pairing DCS with near-infrared spectroscopy (NIRS), an established noninvasive technique for characterizing the transport and utilization of oxygen through the microcirculation (4,5,11,15,19,23,39,42,46), allows for simultaneous measurement of oxygen delivery and utilization (determinants of skeletal muscle oxygen consumption) at the level of the microvasculature. Indeed, recent studies performed in our laboratory (3,39,46) demonstrate good concurrent validity between near-infrared diffuse correlation spectroscopy (NIR-DCS) and conventional measures of oxygen delivery (Doppler Ultrasound) and utilization (venous oxygen saturation) during both fixed workload (46) and incremental (39) handgrip exercise. However, it is still unclear whether NIR-DCS can track acute perturbations in oxygen delivery and utilization at the level of the microvasculature.…”

“…In a prior study from our laboratory (46), we attempted to alter microvascular oxygen delivery by manipulating forearm arterial perfusion pressure (by raising the arm above or lowering the arm below the level of the heart) (6,40,45). Whereas bulk conduit brachial artery blood flow (measured by Doppler ultrasound) followed changes in perfusion pressure during arm manipulation, microvascular perfusion was preserved during steady-state handgrip exercise, which we interpreted as evidence of myogenic autoregulation (46). In a separate, more recent NIR-DCS study, we challenged the system using a graded handgrip exercise test, hoping to observe a divergence between oxygen delivery and oxygen extraction at higher workloads (39).…”

Near‐infrared diffuse correlation spectroscopy: the future of non‐invasive assessment of skeletal muscle oxygenation?

“…In this issue of the Journal of Physiology , for the first time in humans, Tucker et al . () undertook to validate the combination of DCS with typical continuous‐wave NIRS technology against conventional O 2 delivery and utilization measurements [Doppler‐derived forearm blood flow (FBF) and venous blood gas analysis] in the working skeletal muscle. The exercise protocol consisted of 4 min of rhythmic handgrip exercise using a handgrip dynamometer (i.e.…”