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LETTER TO THE EDITOR
Near-infrared (NIR) spectroscopy is a noninvasive optical technique that is increasingly used to assess muscle oxygenation during exercise with the assumption that the contribution of skin blood flow to the NIR signal is minor or nonexistent. We tested this assumption in humans by monitoring forearm tissue oxygenation during selective cutaneous vasodilation induced by locally applied heat (n = 6) or indirect whole body heating (i.e., heating subject but not area surrounding NIR probes; n = 8). Neither perturbation has been shown to cause a measurable change in muscle blood flow or metabolism. Local heating (
41°C) caused large increases in the NIR-derived tissue oxygenation signal [before heating = 0.82 ± 0.89 optical density (OD), after heating = 18.21 ± 2.44 OD; P < 0.001]. Similarly, whole body heating (increase internal temperature 0.9°C) also caused large increases in the tissue oxygenation signal (before heating = –0.31 ± 1.47 OD, after heating = 12.48 ± 1.82 OD; P < 0.001). These increases in the tissue oxygenation signal were closely correlated with increases in skin blood flow during both local heating (mean r = 0.95 ± 0.02) and whole body heating (mean r = 0.89 ± 0.04). These data suggest that the contribution of skin blood flow to NIR measurements of tissue oxygenation can be significant, potentially confounding interpretation of the NIR-derived signal during conditions where both skin and muscle blood flows are elevated concomitantly (e.g., high-intensity and/or prolonged exercise).
The following is the abstract of the article discussed in the subsequent letter:
To the Editor: In a recent article, S. L. Davis et al. (1) presented the results of a study investigating the influence of the increase in the skin blood flow on the near-infrared spectroscopy (NIRS)-based measurement of the flexor digitorum muscle oxygenation during local or whole body heating. Tissue oxygenation was measured by a continuous-wave photometer (NIRO 500; Ref. 3).
We agree with the authors on 1) criticizing prior studies for adopting poor methodologies to increase and assess skin blood flow (5, 6); and 2) recognizing the importance to investigate the influence of skin blood flow, once adequately increased and assessed, on the measurement of muscle oxygenation by NIRS. On the other hand, we disagree with the authors on the NIRS methodology (light source-detector spacing and quantification of NIRS parameters) adopted for testing their hypothesis.
As mentioned by the authors, the light source-detector separation affects the contribution of skin; in fact, increasing this separation properly allows the improvement of the sensitivity of measurement and the increase of the probability of looking at oxygenation deep under the tissue surface (10). In addition, it is well known that the depth of light penetration also depends on the thickness of subcutaneous adipose tissue (7, 9). For these reasons, were the authors wise to have used a source-detector distance of 2 cm? This distance is very short, and to convince the readers that the reported results truly refer to the oxygenation changes occurring in the investigated muscle tissue, the authors should have reported the adipose tissue thickness values and the relationship between longer source-detector distances and skin blood flow. Therefore, their generalized conclusion "skin blood flow can contribute significantly to near-infrared-derived measurements of tissue oxygenation in humans" is not supported by adequate experimental NIRS data.
The authors expressed their results in optical density (OD; without specifying the considered wavelength) instead of reporting changes in concentration of oxy- and deoxyhemoglobin [expressed in µM*cm or 
µM if a pathlength factor is used (2)]. In addition, we would also point out the inconsistency between the reported extremely high values of OD (up to 18) and the performance of the NIRO 500 (the system is linear over a range of ± 0.7 OD; Ref. 3).
We would like to comment that, since 1998, the investigational NIRO 500 device used in the study is no longer commercially available, and it has been replaced by other instruments (tissue oximeters) that use a fixed source-detector spacing of 4 or 5 cm and offer hemoglobin oxygen saturation values ensuring a more accurate quantitation of the oxygenation changes occurring at muscle level.
In summary, the study on the potential contribution of very high levels of skin blood flow to the muscle NIRS signal is of great interest for better understanding of the potential use of NIRS in exercise physiology. However, this issue is still open and additional studies should be carried out using more recent NIRS methodologies (4, 8), which include suitable light source-detector distances, for investigating deep regions of muscle.
REFERENCES
Regarding the concern that the NIR light source-detector spacing of 2 cm might be too short for the light to penetrate both the skin and the underlying muscle, we disagree that this is a limitation of the protocol. Using this spacing, we previously confirmed that the NIR signal was responsive to changes in forearm muscle tissue oxygenation during brief bouts of graded rhythmic handgrip exercise (2, 4–6) in a setting where skin blood flow and skin metabolism are unchanged (7), suggesting that the light penetrates deeply enough to reach the active muscle. In each subject in our current study (3), we confirmed that a brief handgrip evoked forearm deoxygenation to verify the appropriate positioning of the NIR probes over the flexor digitorum profundus muscle. Because the maximal depth of penetration of NIR light is approximately one-half the distance between source and detector, the observed deoxygenation during the brief handgrip would suggest that the thickness of the skin and adipose tissue layers of the young, healthy subjects participating in our study were low. Indeed, van Beekvelt and colleagues previously reported that the average thickness of forearm skin and adipose tissue layers was <3 mm in one study of 26 subjects and <4 mm in another study of 78 subjects (8, 9). Taken together, these previous studies indicate that tissue oxygenation of forearm muscle can be assessed using a source-detector distance of 2 cm, but as our recent work demonstrates, this signal could be greatly influenced by skin blood flow (3).
Finally, we note that Buono et al. (1) recently published a study in which NIR-derived tissue oxyhemoglobin concentrations were increased by local heating-induced elevations in thigh skin blood flow and were decreased by intradermal injection of epinephrine. On the basis of our findings coupled with those of Buono and colleagues, we encourage investigators to consider the potential influence of skin blood flow in the design and interpretation of future studies involving the use of NIR-derived measurements of tissue oxygenation.
REFERENCES
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