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Reply to Quaresima and Ferrari

2009; American Physiological Society; Volume: 107; Issue: 1 Linguagem: Inglês

10.1152/japplphysiol.00314.2009

8750-7587

Andrew M. Jones, Rosemary C. Davies, Leonardo F. Ferreira, Thomas J. Barstow, Shunsaku Koga, David C. Poole,

Cardiovascular Function and Risk Factors

LETTERS TO THE EDITORReply to Quaresima and FerrariAndrew M. Jones, Rosemary C. Davies, Leonardo F. Ferreira, Thomas J. Barstow, Shunsaku Koga, and David C. PooleAndrew M. Jones, Rosemary C. Davies, Leonardo F. Ferreira, Thomas J. Barstow, Shunsaku Koga, and David C. PoolePublished Online:01 Jul 2009https://doi.org/10.1152/japplphysiol.00314.2009MoreSectionsPDF (266 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations to the editor: We thank Drs. Quaresima and Ferrari (16) for alerting us to their disquiet regarding our statement that HHb (deoxygenated hemoglobin) is “relatively insensitive to blood volume changes during exercise and thus reflects the balance between O2 delivery and utilization.” However, we find their position—that this might misrepresent their previous written statements—puzzling, since Fig. 4 in the review cited (6) clearly shows that the O2-Hb signal during exercise demonstrates non-physiological behavior as it tracks changes in total hemoglobin and remains displaced from rest during the prolonged recovery intervals (10+ min). In contrast, the simultaneously measured HHb follows the expected profile of increased arteriovenous O2 difference. Moreover, in papers coauthored by Quaresima and Ferrari (e.g., Ref. 10), muscle oxygenation during exercise transitions is presented as HHb and used as the basis for their on-kinetics analysis.We base our position that HHb provides a more accurate representation of muscle (de)oxygenation (or fractional O2 extraction) during dynamic exercise than does O2-Hb or the tissue oxygenation index (TOI), on a wealth of theoretical reasoning and empirical observations that includes: O2-Hb profiles at the onset of exercise evince pronounced undershoots in healthy young subjects that are absent from direct measurements of fractional O2 extraction in humans (11, 13, 14) and dogs (8) and from microvascular PO2 measurements in rat muscle (1). That HHb best exemplifies the profile of microvascular (de)oxygenation that is reflective of the dynamic balance between O2 delivery and O2 utilization during dynamic exercise is evident in Fig. 1, which demonstrates strikingly similar temporal profiles of changes in muscle intracellular PO2, microvascular PO2, a-vO2 difference, and HHb. Unpublished findings from Drs. Ooue, Koga, and Kondo indicate that skin perfusion, which is altered as a function of core temperature, confounds O2-Hb to a greater extent than HHb. During exercise, the elevation of core temperature increases skin perfusion and blood volume, so that the proportional contribution of skin O2-Hb to the NIRS signal is expected to rise, obscuring changes in muscle O2-Hb (see also Refs. 6, 14). TOI responded in a similar fashion to changes in skin blood flow in the forearm (5) and leg (3). While the source-detector distance we used (4) might help minimize the problem of using TOI as a proxy of fractional O2 extraction dynamics, it does not eliminate it because light still has to go through the skin. The problem of NIRS signal “contamination” by skin blood flow will be minimized for HHb since proportionally much less signal emerges from the skin. This is supported by the independence of HHb kinetics to source-detector spacing, which is proportional to penetration depth (12a).Other points raised by Quaresima and Ferrari (16) also warrant a riposte. First, the use of spatially resolved NIRS methodology to yield high signal-to-noise ratio and lessen the contribution of superficial layers to the TOI signal applies also to the HHb data. Second, changes in total hemoglobin were not different between conditions in our study (Fig. 3C in Ref. 4) such that the use of HHb to reflect muscle O2 extraction is not invalidated. Third, multiplying the HHb data by the same “constant” (assumed value of differential pathlength factor) to provide an “absolute” value will not change the interpretation of our data. Indeed, we consider the latter to be misleading because it would suggest that we actually measured absolute concentrations of HHb when this is not possible with the NIRS technology employed in our study.In summary, we remain resolute in our view that the altered kinetics of HHb adaptation following exercise-induced muscle damage can be correctly interpreted as evidence that muscle fractional O2 extraction was impaired in the transition to high-intensity exercise and that compensatory changes in local blood flow were necessary to enable O2 uptake dynamics to be preserved (4). Fig. 1.Temporal profiles of variables related to altered muscle fractional O2 extraction following the onset of contractions (initiated at time 0) determined using a range of different techniques. Data from Hogan (12), Behnke et al. (2), Grassi et al. (9–11). Note close correspondence in profile of HHb (muscle deoxygenation ) measured by NIRS (bottom right) with all others. Redrawn from Grassi (7).Download figureDownload PowerPointREFERENCES1 Behnke BJ, Kindig CA, Musch TI, Koga S, Poole DC. Dynamics of muscle microvascular oxygen pressure across the rest-exercise transition. Respir Physiol 126: 53–63, 2001.Crossref | PubMed | Google Scholar2 Behnke BJ, Kindig CA, Musch TI, Sexton WL, Poole DC. Effects of prior contractions on muscle microvascular oxygen pressure at onset of subsequent contractions. J Physiol 593: 927–934, 2002.Google Scholar3 Buono MJ, Miller PW, Hom C, Pozos RS, Kolkhorst FW. Skin blood flow affects in vivo near-infrared spectroscopy measurements in human skeletal muscle. Jpn J Physiol 55: 241–244, 2005.Crossref | PubMed | Google Scholar4 Davies RC, Eston RG, Poole DC, Rowlands AV, DiMenna F, Wilkerson DP, Twist C, Jones AM. Effect of eccentric exercise-induced muscle damage on the dynamics of muscle oxygenation and pulmonary oxygen uptake. J Appl Physiol 105: 1413–1421, 2008.Link | ISI | Google Scholar5 Davis SL, Fadel PJ, Cui J, Thomas GD, Crandall CG. Skin blood flow influences near-infrared spectroscopy-derived measurements of tissue oxygenation during heat stress. J Appl Physiol 100: 221–224, 2006.Link | ISI | Google Scholar6 Ferrari M, Binzoni T, Quaresima V. Oxidative metabolism in muscle. Philos Trans R Soc Lond B Biol Sci 352: 677–683, 1997.Crossref | PubMed | ISI | Google Scholar7 Grassi B. Limitation of muscle V̇O2 by cellular respiration. In: Oxygen Uptake Kinetics in Sport, Exercise and Medicine, edited by Jones AM and Poole DC. New York: Routledge, 2005.Google Scholar8 Grassi B, Gladden LB, Samaja M, Stary CM, Hogan MC. Faster adjustment of O2 delivery does not affect on-kinetics in isolated in situ canine muscle. J Appl Physiol 85: 1394–1403, 1998.Link | ISI | Google Scholar9 Grassi B, Hogan MC, Greenhaff PL, Hamann JJ, Kelley KM, Aschenbach WG, Constantin-Teodosiu D, Gladden LB. V̇o2 on-kinetics in dog gastrocnemius in situ following activation of pyruvate dehydrogenase by dichloroacetate. J Physiol 538: 195–207, 2002.Crossref | PubMed | ISI | Google Scholar10 Grassi B, Pogliaghi S, Rampichini S, Quaresima V, Ferrari M, Marconi C, Cerretelli P. Muscle oxygenation and pulmonary gas exchange kinetics during cycling exercise on-transitions in humans. J Appl Physiol 95: 149–158, 2003.Link | ISI | Google Scholar11 Grassi B, Poole DC, Richardson RS, Knight DR, Erickson BK, Wagner PD. Muscle O2 uptake kinetics in humans: implications for metabolic control. J Appl Physiol 80: 988–998, 1996.Link | ISI | Google Scholar12 Hogan MC. Fall in intracellular PO2 at the onset of contractions in Xenopus single muscle fibers. J Appl Physiol 90: 1871–1876, 2001.Link | ISI | Google Scholar12a Horiuchi M, Kowalchuk J. Heterogeneity of muscle deoxygenation kinetics during constant-load moderate- and heavy-exercise. Med Sci Sports Exerc 40, Suppl S117, 2008.Crossref | ISI | Google Scholar13 Koga S, Poole DC, Shiojiri T, Kondo N, Fukuba Y, Miura A, Barstow TJ. A comparison of oxygen uptake kinetics during knee extension and cycle exercise. Am J Physiol Regul Integr Comp Physiol 288: R212–R220, 2005.Link | ISI | Google Scholar14 Maehara K, Riley M, Galasetti P, Barstow TJ, Wasserman K. Effect of hypoxia and carbon monoxide on muscle oxygenation during exercise. Am J Crit Care 155: 229–235, 1997.Crossref | ISI | Google Scholar16 Quaresima V, Ferrari M. Muscle oxygenation by near-infrared-based tissue oximeters. J Appl Physiol doi:10.1152/japplphysiol.00215.2009.Link | ISI | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: A. M. Jones, Univ. of Exeter, Exeter, UK (e-mail: [email protected]) Download PDF Previous Back to Top FiguresReferencesRelatedInformation Cited ByBlood volume versus deoxygenated NIRS signal: computational analysis of the effects muscle O2 delivery and blood volume on the NIRS signalsB. Koirala, A. Concas, Yi Sun, L. B. Gladden, and N. 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