Abstract
Laser Doppler flowmetry (LDF) is used to study skin microcirculation, providing a nonstationary signal which can be simplified with tools such as the wavelet transform (WT), detrended fluctuation analysis (DFA), and multiscale entropy analysis (MSE). WT splits the LDF signal into its main frequency components: heart, respiration, myogenic, sympathetic, and metabolic; DFA determines the α coefficient, which can translate correlations, and MSE quantifies the complexity of the signal over multiple time scales. We characterized the LDF signal obtained during a lower limb occlusion maneuver performed on young adults. Results revealed that the LDF signal is predominantly of sympathetic and metabolic origin, showing different correlation and entropy profiles during the different phases of the protocol. Occlusion significantly changed the components’ amplitude ratios, entropy values, and α exponents. The heart and respiration components showed 1/f noise-like behavior, and the myogenic, sympathetic, and metabolic components showed Brownian noise-like behavior. The combined use of these tools helps to better understand the LDF signal, with an aim to improve its clinical and diagnostic utility.
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Abu-Own A, Scurr JH, Coleridge Smith PD. Effect of leg elevation on the skin microcirculation in chronic venous insufficiency. J Vasc Surg Off Publ Soc Vasc Surg Int Soc Cardiovasc Surg N Am Chapter. 1994;20(5):705–10.
Anderson JL, Halperin JL, Albert N, Bozkurt B, Brindis RG, Curtis LH, et al. Management of patients with peripheral artery disease (compilation of 2005 and 2011 ACCF/AHA guideline recommendations): a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2013;61(14):1555–70.
Aoki K, Stephens DP, Saad AR, Johnson JM. Cutaneous vasoconstrictor response to whole body skin cooling is altered by time of day. J Appl Physiol. 2003;94:930–4.
Bernjak A, Clarkson PB, McClintock PV, Stefanovska A. Microvasc Res. 2008;76(3):224–32.
Berry KL, Skyrme-Jones RA, Meredith IT. Occlusion cuff position is an important determinant of the time course and magnitude of human brachial artery flow-mediated dilation. Clin Sci Lond Engl 1979. 2000;99(4):261–7.
Braverman I. REVIEW the cutaneous microcirculation: ultrastructure and microanatomical organization. Microcirculation. 1997;4(3):329–40.
Charkoudian N, Johnson JM. Female reproductive hormones and thermoregulatory control of skin blood flow. Exerc Sport Sci Ver. 2000;28:108–12.
Costa M, Goldberger AL, Peng CK. Multiscale entropy analysis of complex physiologic time series. Phys Rev Lett. 2002;89:062102.
Cracowski JL, Minson CT, Salvat-Melis M, Halliwill JR. Methodological issues in the assessment of skin microvascular endothelial function in humans. Trends Pharmacol Sci. 2006;27(9):503–8.
Crawford P, Good PA, Gutierrez E, Feinberg JH, Boehmer JP, Silber DH, Sinoway LI. Effects of supplemental oxygen on forearm vasodilation in humans. J Appl Physiol (Bethesda Md). 1985;82(5):1601–6.
Cui J, Arbab-Zadeh A, Prasad A, Durand S, Levine BD, Crandall CG. Effects of heat stress on thermoregulatory responses in congestive heart failure patients. Circulation. 2005;112:2286–92.
Dakak N, Husain S, Mulcahy D, Andrews NP, Panza JA, Waclawiw M, Schenke W, Quyyumi AA. Contribution of nitric oxide to reactive hyperemia: impact of endothelial dysfunction. Hypertension. 1998;32(1):9–15.
Deanfield JE, Halcox JP, Rabelink TJ. Endothelial function and dysfunction: testing and clinical relevance. Circulation. 2007;115(10):1285–95.
Eke A, Herman P, Kocsis L, Kozak L. Fractal characterization of complexity in temporal physiological signals. Physiol Meas. 2002;23(1):R1–38.
Esen F, Esen H. Detrended fluctuation analysis of laser Doppler flowmetry time series: the effect of extrinsic and intrinsic factors on the fractal scaling of microvascular blood flow. Physiol Meas. 2006;27(11):1241–53.
Ferreira HA, Fernandes CD, Pinto PC, Rodrigues LM. Use of wavelet transforms and detrended fluctuation analysis in the evaluation of human skin microcirculation. Biomed Biopharm Res. 2011;1(9):79–86.
Guerreschi E, Humeau-Heurtier A, Bricq S, Mahe G, Lefheriotis G. Proceedings of the 20th European Signal Processing Conference (EUSIPCO). 2012.
Harward TR, Volny J, Golbranson, Bernstein EF, Fronek A. Oxygen inhalation-induced transcutaneous. J Vasc Surg. 1985;2:220–7.
Holowatz LA, Thompson-Torgerson CS, Kenney WL. The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol. 2008;105(1):370–2.
Husmann M, Willenberg T, Keo HH, Spring S, Kalodiki E, Delis KT. Integrity of venoarteriolar reflex determines level of microvascular skin flow enhancement with intermittent pneumatic compression. J Vasc Surg. 2008;48(6):1509–13.
Johnson JM, Proppe DW. Cardiovascular adjustments to heat stress. In: Handbook of physiology. Environ Physiol. 1996;215–43, Am Physiol Soc, Bethesda.
Khan F, Litchfield SJ, Stonebridge PA, Belch JJ. Lipid-lowering and skin vascular responses in patients with hypercholesterolaemia and peripheral arterial obstructive disease. Vasc Med. 1999;4:233–8.
Landsverk SV, Kvandal P, Bernjak A, Ste- fanovska A, Kirkeboen KA. The effects of general anesthesia on human skin microcirculation evaluated by wavelet transform. Anesth Analg. 2007;105:1012–9.
Lenasi H. Assessment of human skin microcirculation and its endothelial function using laser Doppler flowmetry. In: Erondu OF, editor. Medical imaging. Rijeka: InTech; 2011. p. 271–96.
Levy BI, Ambrosio G, Pries AR, Struijker-Boudier HA. Microcirculation in hypertension: a new target for treatment? Circulation. 2001;104(6):735–40.
Minson CT. Thermal provocation to evaluate microvascular reactivity in human skin. J Appl Physiol. 2010;109:1239–46.
Minson CT, Holowatz LA, Wong BJ, Kenney WL, Wilkins BW. Decreased nitric oxide- and axon reflex-mediated cutaneous vasodilation with age during local heating. J Appl Physiol (Bethesda Md). 1985;93(5):1644–9.
Morales F, Graaff R, Smit AJ, Bertuglia S, Petoukhova AL, Steenbergen W, Rakhorst G. How to assess post-occlusive reactive hyperaemia by means of laser Doppler perfusion monitoring: application of a standardised protocol to patients with peripheral arterial obstructive disease. Microvasc Res. 2005;69(1–2):17–23.
Morris SJ, Shore AC. Skin blood flow responses to the iontophoresis of acetylcholine and sodium nitroprusside in man: possible mechanisms. J Physiol. 1996;496(Pt 2):531–42.
Peng CK, Buldyrev SV, Havlin S, Simons M, Stanley HE, Goldberger AL. Mosaic organization of DNA nucleotides. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1994;49(2):1685–9.
Peng CK, Havlin S, Stanley HE, Goldberger AL. Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos. 1995;5(1):82–90.
Rizzoni D, Porteri E, Boari GE, DeCiuceis C, Sleiman I, Muiesan ML, et al. Prognostic significance of small-artery structure in hypertension. Circulation. 2003;108:2230–5.
Roddie IC. Circulation to skin and adipose tissue. In: Geiger S, editor. The cardiovascular system. Am Physiol Soc. 1983;285–317.
Rossi M, Carpi A. Skin microcirculation in peripheral arterial obliterative disease. Biomed Pharmacother. 2004;58(8):427–31.
Rossi M, Carpi A, Di Maria C, Galetta F, Santoro G. Spectral analysis of laser Doppler skin blood flow oscillations in human essential hypertension. Microvasc Res. 2006;72(1–2):34–41.
Sacks AH, Ksander G, O’Neill H, Perkash I. Difficulties in laser Doppler measurement of skin blood flow under applied external pressure. J Rehabil Res Dev. 1988;25(3):19–24.
Saumet JL, Kellogg Jr DL, Taylor WF, Johnson JM. Cutaneous laser-Doppler flowmetry: influence of underlying muscle blood flow. J App Physiol. 1988;65(1):478–81.
Sax FL, Cannon RO, Hanson C, Epstein SE. Impaired forearm vasodilator reserve in patients with microvascular angina. Evidence of a generalized disorder of vascular function? N Engl J Med. 1987;317:1366–70.
Schubert V. The influence of local heating on skin microcirculation in pressure ulcers, monitored by a combined laser Doppler and transcutaneous oxygen tension probe. Clin Physiol (Oxford England). 2000;20(6):413–21.
Shamim-Uzzaman QA, Pfenninger D, Kehrer C, Chakrabarti A, Kacirotti N, Rubenfire M, et al. Altered cutaneous microvascular responses to reactive hyperaemia in coronary artery disease: a comparative study with conduit vessel responses. Clin Sci. 2002;103(3):267–73.
Sifuzzaman M, Islam MR, Ali MZ. Application of wavelet transform and its advantages compared to Fourier transform. J Phys Sci. 2009;13:121–34.
Silva H, Ferreira H, Tavares L, Bujan J, Rod-rigues LM. Exploring in vivo models to characterize peripheral microcirculation – a pilot study. Biomed Biopharm Res. 2013a;10(1):65–72.
Silva H, Ferreira H, Bujan J, Rodrigues LM. Exploring the oxygen challenge test as a microcirculation evaluation model. Biomed Biopharm Res. 2013b;10(2):209–15.
Sokolnicki LA, Roberts SK, Wilkins BW, Basu A, Charkoudian N, et al. Contribution of nitric oxide to cutaneous microvascular dilation in individuals with type 2 diabetes mellitus. Am J Physiol Endocrinol Metab. 2006;292:E314–8.
Srinivasa G, Sujatha N. Fractal dimension characterization of in-vivo laser Doppler flowmetry signals. Phys Procedia. 2011;19:49–54.
Stewart J, Kohen A, Brouder D, Rahim F, Adler S, Garrick R, Goligorsky MS. Noninvasive interrogation of microvasculature for signs of endothelial dysfunction in patients with chronic renal failure. Am J Physiol Heart Circ Physiol. 2004;287:H2687–E2696.
Thompson-torgerson CS, Holowatz LA, Flavahan NA, Kenney WL. Rho kinase-mediated local cold-induced cutaneous vasoconstriction is augmented in aged human skin. Am J Physiol Heart Circ Physiol. 2007;293(1):H30–6.
Verdant C, De Backer D. How monitoring of the microcirculation may help us at the bedside. Curr Opin Crit Care. 2005;11:240–4.
World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA : J Am Med Assoc. 2013;310(20):2191–4.
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Silva, H., Ferreira, H., Rodrigues, L.M. (2015). Studying the Oscillatory Components of Human Skin Microcirculation. In: Humbert, P., Maibach, H., Fanian, F., Agache, P. (eds) Measuring the Skin. Springer, Cham. https://doi.org/10.1007/978-3-319-26594-0_62-1
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DOI: https://doi.org/10.1007/978-3-319-26594-0_62-1
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