Suitability of the muscle O2 resaturation parameters most used for assessing reactive hyperemia: a near-infrared spectroscopy study

Gustavo Vieira de Oliveira; Mônica Volino-Souza; Renata Leitão; Vivian Pinheiro; Carlos Adam Conte-Júnior; Thiago Silveira Alvares

doi:10.1590/1677-5449.200143

Original Article

Suitability of the muscle O₂ resaturation parameters most used for assessing reactive hyperemia: a near-infrared spectroscopy study

Adequação de parâmetros de ressaturação muscular de O₂ mais utilizados na avaliação da hiperemia reativa: um estudo por espectroscopia no infravermelho próximo

Gustavo Vieira de Oliveira; Mônica Volino-Souza; Renata Leitão; Vivian Pinheiro; Carlos Adam Conte-Júnior; Thiago Silveira Alvares

http://dx.doi.org/10.1590/1677-5449.200143 J Vasc Bras, vol.20, e20200143, 2021

PDF

SciELO

Downloads: 2

Abstract

Abstract: Background: There is a spectrum of possibilities for analyzing muscle O₂ resaturation parameters for measurement of reactive hyperemia in microvasculature. However, there is no consensus with respect to the responsiveness of these O₂ resaturation parameters for assessing reactive hyperemia.

Objectives: This study investigates the responsiveness of the most utilized muscle O₂ resaturation parameters to assess reactive hyperemia in the microvasculature of a clinical group known to exhibit impairments of tissue O₂ saturation (StO₂).

Methods: Twenty-three healthy young adults, twenty-nine healthy older adults, and thirty-five older adults at risk of cardiovascular disease (CVD) were recruited. Near-infrared spectroscopy (NIRS) was used to assess StO₂ after a 5-min arterial occlusion challenge and the following parameters were analyzed: StO_{2slope_10s}, StO_{2slope_30s}, and StO_{2slope_until_baseline} (upslope of StO₂ over 10s and 30s and until StO₂ reaches the baseline value); time to StO_2baseline and time to StO_2max (time taken for StO₂ to reach baseline and peak values, respectively); ∆StO_2reperfusion (the difference between minimum and maximum StO₂ values); total area under the curve (StO_2AUCt); and AUC above the baseline value (StO_{2AUC_above_base}).

Results: Only StO_{2slope_10s} was significantly slower in older adults at risk for CVD compared to healthy young individuals (p < 0.001) and to healthy older adults (p < 0.001). Conversely, time to StO_2max was significantly longer in healthy young individuals than in older adult at CVD risk.

Conclusions: Our findings suggest that StO_{2slope_10s} may be a measure of reactive hyperemia, which provides clinical insight into microvascular function assessment.

Keywords

cardiovascular physiology, capillary endothelial cells, vascular disease, hypertension, aging

Resumo

Resumo: Contexto: Existe um espectro de possibilidades na análise dos parâmetros de ressaturação de O₂ muscular como uma medida de hiperemia reativa na microvasculatura. No entanto, não há consenso com relação à responsividade desses parâmetros de ressaturação de O₂ para avaliação de hiperemia reativa.

Objetivos: Este estudo investigou a capacidade de resposta dos parâmetros de ressaturação muscular de O₂ mais utilizados para avaliar a hiperemia reativa na microvasculatura de um grupo clínico conhecido por apresentar comprometimento da saturação de O₂ (StO₂).

Métodos: Foram recrutados 23 jovens saudáveis, 29 idosos saudáveis e 35 idosos com risco para doença cardiovascular. A espectroscopia no infravermelho próximo foi usada para avaliar a StO₂ após um teste de oclusão arterial de 5 minutos, no qual os seguintes parâmetros foram analisados: StO_{2slope_10s}, StO_{2slope_30s} e StO2_{slope_until_baseline} (inclinação da StO₂ em 10 s, 30 s e até StO₂ atingir valores basais); tempo para StO_2baseline e tempo para StO_2máx (o tempo necessário para StO₂ atingir os valores da linha de base e o máximo, respectivamente); ∆StO_2reperfusão (a diferença entre o valor de StO_2mínimo e StO_2máximo); área total sob a curva (StO_2AUCt); e área sob a curva acima do valor da linha de base (StO_{2AUC_above_base}).

Resultados: Apenas StO_{2slope_10s} foi significativamente mais lento em idosos em risco de doença cardiovascular comparados com indivíduos jovens saudáveis (p < 0,001) e idosos saudáveis (p < 0,001). Por outro lado, o tempo para StO_2max foi significativamente maior em indivíduos jovens saudáveis do que em idosos em risco de doença cardiovascular.

Conclusões: Nossos achados sugerem que StO_{2slope_10s} pode ser uma medida de hiperemia reativa, que fornece informações clínicas sobre a avaliação da função microvascular.

Palavras-chave

fisiologia cardiovascular, células endoteliais capilares, doenças vasculares, hipertensão arterial, envelhecimento

References

1 Martin BJ, Anderson TJ. Risk prediction in cardiovascular disease: the prognostic significance of endothelial dysfunction. Can J Cardiol. 2009;25(Suppl A):15A-20A. http://dx.doi.org/10.1016/S0828-282X(09)71049-9. PMid:19521569.

2 Thijssen DHJ, Bruno RM, van Mil ACCM, et al. Expert consensus and evidence-based recommendations for the assessment of flow-mediated dilation in humans. Eur Heart J. 2019;40(30):2534-47. http://dx.doi.org/10.1093/eurheartj/ehz350. PMid:31211361.

3 Rosenberry R, Nelson MD. Reactive hyperemia: a review of methods, mechanisms, and considerations. Am J Physiol Regul Integr Comp Physiol. 2020;318(3):R605-18. http://dx.doi.org/10.1152/ajpregu.00339.2019. PMid:32022580.

4 Dipla K, Triantafyllou A, Koletsos N, et al. Impaired Muscle Oxygenation and Elevated Exercise Blood Pressure in Hypertensive Patients: Links With Vascular Stiffness. Hypertension. 2017;70(2):444-51. http://dx.doi.org/10.1161/HYPERTENSIONAHA.117.09558. PMid:28607132.

5 Parmenter BJ, Mavros Y, Ritti Dias R, King S, Fiatarone Singh M. Resistance training as a treatment for older persons with peripheral artery disease: a systematic review and meta-analysis. Br J Sports Med. 2020;54(8):452-61. PMid:30979698.

6 Ferrari M, Mottola L, Quaresima V. Principles, techniques, and limitations of near infrared spectroscopy. Can J Appl Physiol. 2004;29(4):463-87. http://dx.doi.org/10.1139/h04-031. PMid:15328595.

7 de Oliveira GV, Volino-Souza M, Leitão R, Pinheiro V, Alvares TS. Is flow-mediated dilatation associated with near-infrared spectroscopy-derived magnitude of muscle O₂ desaturation in healthy young and individuals at risk for cardiovascular disease? Microvasc Res. 2020;129:103967. http://dx.doi.org/10.1016/j.mvr.2019.103967. PMid:31837305.

8 McLay KM, Fontana FY, Nederveen JP, et al. Vascular responsiveness determined by near-infrared spectroscopy measures of oxygen saturation. Exp Physiol. 2016;101(1):34-40. http://dx.doi.org/10.1113/EP085406. PMid:26498127.

9 Oliveira GV, Soares RN, Volino-Souza M, Murias JM, Alvares TS. The association between near-infrared spectroscopy assessment of microvascular reactivity and flow-mediated dilation is disrupted in individuals at high risk for cardiovascular disease. Microcirculation. 2019;26(7):e12556. http://dx.doi.org/10.1111/micc.12556. PMid:31077636.

10 de Oliveira GV, Soares RN, Volino-Souza M, Leitão R, Murias JM, Alvares TS. The effects of aging and cardiovascular risk factors on microvascular function assessed by near-infrared spectroscopy. Microvasc Res. 2019;126:103911. http://dx.doi.org/10.1016/j.mvr.2019.103911. PMid:31425692.

11 Soares RN, Somani YB, Proctor DN, Murias JM. The association between near-infrared spectroscopy-derived and flow-mediated dilation assessment of vascular responsiveness in the arm. Microvasc Res. 2019;122:41-4. http://dx.doi.org/10.1016/j.mvr.2018.11.005. PMid:30445134.

12 Papadopoulos S, Dipla K, Triantafyllou A, et al. Beetroot increases muscle performance and oxygenation during sustained isometric exercise, but does not alter muscle oxidative efficiency and microvascular reactivity at rest. J Am Coll Nutr. 2018;37(5):361-72. http://dx.doi.org/10.1080/07315724.2017.1401497. PMid:29425473.

13 Townsend DK, Deysher DM, Wu EE, Barstow TJ. Reduced insulin sensitivity in young, normoglycaemic subjects alters microvascular tissue oxygenation during postocclusive reactive hyperaemia. Exp Physiol. 2019;104(6):967-74. http://dx.doi.org/10.1113/EP087216. PMid:31020733.

14 Dipla K, Triantafyllou A, Grigoriadou I, et al. Impairments in microvascular function and skeletal muscle oxygenation in women with gestational diabetes mellitus: links to cardiovascular disease risk factors. Diabetologia. 2017;60(1):192-201. http://dx.doi.org/10.1007/s00125-016-4129-7. PMid:27722775.

15 Le Roux-Mallouf T, Vibert F, Doutreleau S, Verges S. Effect of acute nitrate and citrulline supplementation on muscle microvascular response to ischemia-reperfusion in healthy humans. Appl Physiol Nutr Metab. 2017;42(9):901-8. http://dx.doi.org/10.1139/apnm-2017-0081. PMid:28460182.

16 Ramos Gonzalez M, Caldwell JT, Branch PA, et al. Impact of shear rate pattern on post-occlusive near-infrared spectroscopy microvascular reactivity. Microvasc Res. 2018;116:50-6. http://dx.doi.org/10.1016/j.mvr.2017.10.004. PMid:29080792.

17 Rosenberry R, Munson M, Chung S, et al. Age-related microvascular dysfunction: novel insight from near-infrared spectroscopy. Exp Physiol. 2018;103(2):190-200. http://dx.doi.org/10.1113/EP086639. PMid:29114952.

18 Kragelj R, Jarm T, Erjavec T, Presern-Strukelj M, Miklavcic D. Parameters of postocclusive reactive hyperemia measured by near infrared spectroscopy in patients with peripheral vascular disease and in healthy volunteers. Ann Biomed Eng. 2001;29(4):311-20. http://dx.doi.org/10.1114/1.1359451. PMid:11339328.

19 Mattu AT, MacInnis MJ, Doyle-Baker PK, Murias JM. Effects of the menstrual and oral contraceptive cycle phases on microvascular reperfusion. Exp Physiol. 2020;105(1):184-91. http://dx.doi.org/10.1113/EP088135. PMid:31625647.

20 Rosenberry R, Trojacek D, Chung S, Cipher DJ, Nelson MD. Interindividual differences in the ischemic stimulus and other technical considerations when assessing reactive hyperemia. Am J Physiol Regul Integr Comp Physiol. 2019;317(4):R530-8. http://dx.doi.org/10.1152/ajpregu.00157.2019. PMid:31314545.

21 Tremblay JC, King TJ. Near-infrared spectroscopy: can it measure endothelial function? Exp Physiol. 2016;101(11):1443-4. http://dx.doi.org/10.1113/EP085902. PMid:27620539.

22 Soares RN, Oliveira GV, Alvares TS, Murias JM. The effects of the analysis strategy on the correlation between the NIRS reperfusion measures and the FMD response. Microvasc Res. 2020;127:103922. http://dx.doi.org/10.1016/j.mvr.2019.103922. PMid:31479661.

23 Ryan TE, Brophy P, Lin CT, Hickner RC, Neufer PD. Assessment of in vivo skeletal muscle mitochondrial respiratory capacity in humans by near-infrared spectroscopy: a comparison with in situ measurements. J Physiol. 2014;592(15):3231-41. http://dx.doi.org/10.1113/jphysiol.2014.274456. PMid:24951618.

24 Gayda M, Juneau M, Tardif JC, Harel F, Levesque S, Nigam A. Cardiometabolic and traditional cardiovascular risk factors and their potential impact on macrovascular and microvascular function: preliminary data. Clin Hemorheol Microcirc. 2015;59(1):53-65. http://dx.doi.org/10.3233/CH-141816. PMid:24518371.

25 Soares RN, Proctor DN, Oliveira GV, Alvares TS, Murias JM. Acute application of a transdermal nitroglycerin patch protects against prolonged forearm ischemia‐induced microvascular dysfunction. Microcirculation. 2020;27(3):e12599. http://dx.doi.org/10.1111/micc.12599. PMid:31782855.

26 Grassi B, Quaresima V. Near-infrared spectroscopy and skeletal muscle oxidative function in vivo in health and disease: a review from an exercise physiology perspective. J Biomed Opt. 2016;21(9):091313. http://dx.doi.org/10.1117/1.JBO.21.9.091313. PMid:27443955.

27 van Beekvelt MC, Borghuis MS, van Engelen BG, Wevers RA, Colier WN. Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci. 2001;101(1):21-8. http://dx.doi.org/10.1042/cs1010021. PMid:11410110.

Submitted date:
08/14/2020

Accepted date:
10/12/2020

Sociedade Brasileira de Angiologia e Cirurgia Vascular (SBACV)"> Sociedade Brasileira de Angiologia e Cirurgia Vascular (SBACV)">

Suitability of the muscle O2 resaturation parameters most used for assessing reactive hyperemia: a near-infrared spectroscopy study

Adequação de parâmetros de ressaturação muscular de O2 mais utilizados na avaliação da hiperemia reativa: um estudo por espectroscopia no infravermelho próximo