Assessment of power spectral density of microvascular hemodynamics in skeletal muscles at very low and low-frequency via near-infrared diffuse optical spectroscopies

Caterina Amendola; Mauro Buttafava; Talyta Carteano; Letizia Contini; Lorenzo Cortese; Turgut Durduran; Turgut Durduran; Lorenzo Frabasile; Claudia Nunzia Guadagno; Umut Karadeniz; Michele Lacerenza; Jaume Mesquida; Shahrzad Parsa; Rebecca Re; Rebecca Re; Diego Sanoja Garcia; Sanathana Konugolu Venkata Sekar; Lorenzo Spinelli; Alessandro Torricelli; Alessandro Torricelli; Alberto Tosi; Udo M. Weigel; M. Atif Yaqub; Marta Zanoletti; Davide Contini

doi:10.1364/BOE.502618

Biomedical Optics Express
Vol. 14,
Issue 11,
pp. 5994-6015
(2023)
•https://doi.org/10.1364/BOE.502618

Assessment of power spectral density of microvascular hemodynamics in skeletal muscles at very low and low-frequency via near-infrared diffuse optical spectroscopies

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Caterina Amendola, Mauro Buttafava, Talyta Carteano, Letizia Contini, Lorenzo Cortese, Turgut Durduran, Lorenzo Frabasile, Claudia Nunzia Guadagno, Umut Karadeniz, Michele Lacerenza, Jaume Mesquida, Shahrzad Parsa, Rebecca Re, Diego Sanoja Garcia, Sanathana Konugolu Venkata Sekar, Lorenzo Spinelli, Alessandro Torricelli, Alberto Tosi, Udo M. Weigel, M. Atif Yaqub, Marta Zanoletti, and Davide Contini, "Assessment of power spectral density of microvascular hemodynamics in skeletal muscles at very low and low-frequency via near-infrared diffuse optical spectroscopies," Biomed. Opt. Express 14, 5994-6015 (2023)

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About this Article
History
- Original Manuscript: August 7, 2023
- Revised Manuscript: October 10, 2023
- Manuscript Accepted: October 16, 2023
- Published: October 26, 2023

Abstract

In this work, we used a hybrid time domain near-infrared spectroscopy (TD-NIRS) and diffuse correlation spectroscopy (DCS) device to retrieve hemoglobin and blood flow oscillations of skeletal muscle microvasculature. We focused on very low (VLF) and low-frequency (LF) oscillations (i.e., frequency lower than 0.145 Hz), that are related to myogenic, neurogenic and endothelial activities. We measured power spectral density (PSD) of blood flow and hemoglobin concentration in four muscles (thenar eminence, plantar fascia, sternocleidomastoid and forearm) of 14 healthy volunteers to highlight possible differences in microvascular hemodynamic oscillations. We observed larger PSDs for blood flow compared to hemoglobin concentration, in particular in case of distal muscles (i.e., thenar eminence and plantar fascia). Finally, we compared the PSDs measured on the thenar eminence of healthy subjects with the ones measured on a septic patient in the intensive care unit: lower power in the endothelial-dependent frequency band, and larger power in the myogenic ones were observed in the septic patient, in accordance with previous works based on laser doppler flowmetry.

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Caterina Amendola, Mauro Buttafava, Talyta Carteano, Letizia Contini, Lorenzo Cortese, Turgut Durduran, Lorenzo Frabasile, Claudia Nunzia Guadagno, Umut Karadeniz, Michele Lacerenza, Jaume Mesquida, Shahrzad Parsa, Rebecca Re, Diego Sanoja Garcia, Sanathana Konugolu Venkata Sekar, Lorenzo Spinelli, Alessandro Torricelli, Alberto Tosi, Udo M. Weigel, M. Atif Yaqub, Marta Zanoletti, and Davide Contini, "Assessment of power spectral density of microvascular hemodynamics in skeletal muscles at very low and low-frequency via near-infrared diffuse optical spectroscopies: erratum," Biomed. Opt. Express 15, 3425-3425 (2024)
https://opg.optica.org/boe/abstract.cfm?uri=boe-15-5-3425

24 April 2024: A correction was made to an author name.

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Data underlying the results presented in this paper are not publicly available at this time but may be obtained from the authors upon reasonable request.

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Fig. 1. Schematic of the probe position during measurements: panel a) forearm, panel b) thenar eminence, panel c) sternocleidomastoid, d) plantar fascia.

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Fig. 2. Time traces of percentage variations of tHb, S_tO₂ (left column) and BFI (right column) measured on thenar eminence (panels (a) and (b)), forearm (panels (c) and (d)), sternocleidomastoid (panels (e) and (f)) and plantar fascia (panels (g) and (h)) of one exemplary healthy volunteer.

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Fig. 3. Zoom of the power spectral density (PSD) highlighting the spectral components at the three intervals of deoxygenated hemoglobin (HHb, panel (a)), oxygenated hemoglobin (HbO₂, panel (b)), total hemoglobin (tHb, panel (c)), tissue oxygen saturation (S_tO₂, panel (d)), averaged among all the participants, in different muscles. Lines are the average values, while shadows are the corresponding standard errors.

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Fig. 4. Power spectral density (PSD) of blood flow index (BFI) averaged among all the participants, in different muscles. Lines are the average values, while shadows are the corresponding standard errors.

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Fig. 5. Power spectral density (PSD) of HHb (panel (a)), HbO₂ (panel (b)), tHb (panel (c)) and S_tO₂ (panel (d)) averaged among all the volunteers (blue line) compared with PSDs measured for the septic patient (yellow line), on the thenar eminence.

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Fig. 6. Power spectral density (PSD) of blood flow index (BFI) averaged among all the volunteers (blue line) compared with PSD of BFI measured on a septic patient (yellow line), on the thenar eminence.

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Fig. 7. Box plot of absolute and relative areas of PSDs measured on the thenar eminence computed in the three intervals of interest in case of healthy subjects (asterisk), compared to the ones measured in the septic patients (red diamond). The red lines inside the boxes represent the median, the bottom and top edges of the box indicate the 25^th and 75^th percentiles, for healthy volunteers. The whiskers extend to the most extreme data points not considered outliers.

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Tables (9)

Table 1. Average and interquartile range (IQR) of age, body mass index (BMI), systolic and diastolic pressure of the healthy participants at the moment of the measurement.

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Table 2. Average and standard deviation (std) of anatomical, optical, and hemodynamic parameters during resting state measurements in four body positions, divided according to the participant sex.

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Table 3. Systolic/diastolic pressure, BMI, age, and average optical and hemodynamic parameters (± their standard deviations) over the 500s acquisition measured on the thenar eminence of the ICU septic patient, at the moment of the enrollment.

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Table 4. p-value computed by Wilcoxon signed-rank test comparing absolute areas of PSD for BFI in different regions of the body, in 14 healthy volunteers. In bold the statistically significant p-value according to Bonferroni correction for multiple comparisons.

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Table 5. p-value computed by Wilcoxon signed-rank test comparing absolute and relative areas of PSD for HHb in different regions of the body, in 14 healthy volunteers. In bold the statistically significant p-value according to Bonferroni correction for multiple comparisons.

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Table 6. p-value computed by Wilcoxon signed-rank test comparing absolute and relative areas of PSD for HbO₂ in different regions of the body, in 14 healthy volunteers. In bold the statistically significant p-value according to Bonferroni correction for multiple comparisons.

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Table 7. p-value computed by Wilcoxon signed-rank test comparing absolute and relative areas of PSD for tHb in different regions of the body, in 14 healthy volunteers. In bold the statistically significant p-value according to Bonferroni correction for multiple comparisons.

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Table 8. p-value computed by Wilcoxon signed-rank test comparing absolute and relative areas of PSD for S_tO₂ in different regions of the body, in 14 healthy volunteers. In bold the statistically significant p-value according to Bonferroni correction for multiple comparisons.

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Table 9. Median and interquartile range of absolute and relative areas of PSD for hemodynamic parameters measured on the thenar eminence of healthy subjects, and same areas measured on the septic patient.

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	All subjects (N = 14)		Female (N = 4)		Male (N = 10)
	Average	IQR	Average	IQR	Average	IQR
Diastolic pressure (mmHg)	71.5	10.5	68	12	72.9	14.7
Systolic pressure (mmHg)	115.8	13	107	14.25	119	10.0
BMI (kg/m²)	21.9	2.5	20.55	1.97	22.44	1.96
Age (years)	27.2	4.5	28.25	4.25	26.8	4.5

		Thenar eminence		Forearm		Sternocleidomastoid		Plantar fascia
		Mean	std	Mean	std	Mean	std	Mean	std
All subjects	Muscle depth (mm)	2.3	0.22	3.11	1.01	2.78	0.77	0.94	0.63
	µ_a,670 (cm⁻¹)	0.38	0.08	0.32	0.07	0.28	0.07	0.14	0.08
	µ_a,830 (cm⁻¹)	0.26	0.06	0.29	0.07	0.26	0.07	0.12	0.05
	µ’_s,670 (cm⁻¹)	7.30	1.3	9.01	1.1	10.61	1.53	11.96	1.4
	µ’_s,830 (cm⁻¹)	5.22	1.1	7.26	1.30	8.85	1.63	11.01	1.64
	tHb (µM)	128.45	29.53	140.22	31.77	127.1	32.73	56.33	22.49
	S_tO₂ (%)	59.90	6.03	72.68	2.76	73.02	4.18	69.88	3.75
	BFI (10⁻⁹cm²/s)	18.3	9.03	7.34	3.5	28.0	20.0	0.83	0.35
Female	Muscle depth (mm)	2.42	0.34	3.83	0.89	3.4	0.36	0.91	0.10
	µ_a,670 (cm⁻¹)	0.37	0.13	0.24	0.04	0.25	0.05	0.14	0.04
	µ_a,830 (cm⁻¹)	0.22	0.06	0.23	0.03	0.22	0.02	0.11	0.02
	µ’_s,670 (cm⁻¹)	6.61	1.3	8.92	0.55	10.71	1.66	11.48	0.91
	µ’_s,830 (cm⁻¹)	4.5	0.41	6.14	0.35	9.21	2.33	10.57	1.06
	tHb (µM)	112.99	32.20	110.47	14.30	106.80	10.64	53.46	12.46
	S_tO₂ (%)	54.39	9.50	73.74	1.98	72.21	4.68	67.54	3.30
	BFI (10⁻⁹cm²/s)	10.7	3.8	6.11	3.77	29.8	28.5	0.68	0.11
Male	Muscle depth (mm)	2.24	0.28	2.83	0.90	2.54	0.83	0.96	0.74
	µ_a,670 (cm⁻¹)	0.38	0.06	0.35	0.07	0.30	0.08	0.14	0.06
	µ_a,830 (cm⁻¹)	0.27	0.05	0.31	0.06	0.28	0.07	0.12	0.05
	µ’_s,670 (cm⁻¹)	7.57	1.04	9.04	1.22	10.56	1.6	12.14	1.45
	µ’_s,830 (cm⁻¹)	5.52	1.02	7.71	1.45	8.71	1.31	11.19	1.73
	tHb (µM)	134.63	24.18	152.11	31.43	135.22	33.46	57.47	24.35
	S_tO₂ (%)	62.10	5.87	72.25	2.84	73.33	4.25	70.81	3.90
	BFI (10⁻⁹cm²/s)	21.3	9.33	7.83	3.4	27.2	15.8	0.89	0.38

Diastolic pressure (mmHg)	55
Systolic pressure (mmHg)	119
BMI (kg/m²)	30.6
Age (years)	61
µ_a,685 (cm⁻¹)	0.20 ± 0.002
µ_a,830 (cm⁻¹)	0.17 ± 0.002
µ’_s,685 (cm⁻¹)	8.03 ± 0.11
µ’_s,830 (cm⁻¹)	6.94 ± 0.10
tHb (µM)	86.3 ± 1.39
S_tO₂ (%)	60.25 ± 1.05
BFI (10⁻⁹cm²/s)	15.1 ± 4.55

		I₁= [0.0095; 0.021] Hz			I₂= [0.021; 0.052] Hz			I₃= [0.052; 0.145] Hz
		Plantar fascia	Sternocleidomastoid	Forearm	Plantar fascia	Sternocleidomastoid	Forearm	Plantar fascia	Sternocleidomastoid	Forearm
Absolute area	Thenar eminence	0.29	0.001	0.0001	0.50	0.0003	0.0001	0.76	0.0002	0.0001
	Plantar fascia	/	0.0001	0.0001	/	0.0001	0.0001	/	0.0001	0.0008
	Sternocleidomastoid	/	/	0.26	/	/	0.42	/	/	0.058

		I₁= [0.0095; 0.021] Hz			I₂= [0.021; 0.052] Hz			I₃= [0.052; 0.145] Hz
		Plantar fascia	Sternocleidomastoid	Forearm	Plantar fascia	Sternocleidomastoid	Forearm	Plantar fascia	Sternocleidomastoid	Forearm
Absolute area	Thenar eminence	0.0001	0.13	0.006	0.006	0.049	0.53	0.0002	0.167	0.008
	Plantar fascia	/	0.0001	0.0001	/	0.0008	0.0001	/	0.002	0.006
	Sternocleidomastoid	/	/	0.07	/	/	0.453	/	/	0.261
Relative area	Thenar eminence	0.0002	0.98	0.013	0.040	0.491	0.572	0.008	0.03	0.03
	Plantar fascia	/	0.0002	0.0001	/	0.889	0.0476		0.0001	0.0001
	Sternocleidomastoid	/	/	0.03	/	/	0.1492			0.53

		I₁= [0.0095; 0.021] Hz			I₂= [0.021; 0.052] Hz			I₃= [0.052; 0.145] Hz
		Median healthy	IQR healthy	Septic patient	Median healthy	IQR healthy	Septic patient	Median healthy	IQR healthy	Septic patient
Absolute area	HHb	0.137	0.046	0.016	0.049	0.019	0.013	0.093	0.028	0.049
	HbO₂	0.094	0.044	0.009	0.088	0.016	0.034	0.156	0.049	0.082
	tHb	0.043	0.015	0.008	0.037	0.018	0.008	0.037	0.010	0.021
	S_tO₂	0.042	0.053	0.003	0.024	0.020	0.012	0.046	0.038	0.032
	BFI	24.469	44.642	6.702	32.092	42.477	18.572	19.297	25.526	26.157
Relative area	HHb	0.133	0.063	0.071	0.050	0.025	0.056	0.079	0.056	0.216
	HbO₂	0.072	0.052	0.023	0.070	0.014	0.085	0.128	0.018	0.205
	tHb	0.161	0.061	0.067	0.121	0.028	0.071	0.144	0.0635	0.179
	S_tO₂	0.088	0.041	0.019	0.053	0.022	0.081	0.111	0.042	0.225
	BFI	0.218	0.070	0.084	0.257	0.071	0.232	0.184	0.099	0.327

Abstract

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