Abstract
Purpose
Functional limitations during exercise from alterations in the balance of oxygen supply and demand—as reported by lower tissue oxygen saturation and longer recovery time—are well documented in clinical populations. We aimed to assess changes in skeletal muscle hemoglobin oxygen saturation (StO2) characteristics during exercise as a result of aging in otherwise healthy individuals.
Methods
We recruited healthy male and female participants (n = 101) from three age ranges—young (18–39 years), middle age (40–65 years), and older (> 65 years)—to complete exercise tests commonly used in clinical populations. Using near-infrared spectroscopy (NIRS) we assessed StO2 in the medial gastrocnemius during the Gardner Treadmill Protocol and 6 min walk test (6MWT).
Results
Minimum StO2 (%) during the treadmill test was significantly lower for both middle-age (36.1 ± 20.6) and older (27.3 ± 19.4) participants compared to young (46.8 ± 14.8) (p < 0.05 and p < 0.01 respectively), and recovery time (minutes) was significantly prolonged (young = 0.22 ± 0.34; middle age = 0.66 ± 0.52; older = 1.04 ± 1.00) (p < 0.001 for both middle age and older compared to young). Similar results were shown during the 6MWT, as minimum StO2 (%) was lower in middle-age (41.7 ± 17.2) and older (40.0 ± 25.9) participants compared to young (53.6 ± 14.5) (p < 0.05), and recovery times (minutes) were prolonged (young: 0.11 ± 0.17; middle age: 0.46 ± 0.42; older: 0.93 ± 0.43) (p < 0.001 for both middle age and older compared to young). Simple linear regression analyses demonstrated that age predicted treadmill recovery and 6MWT recovery.
Conclusion
Our study provides evidence that aging, even in otherwise healthy individuals, negatively impacts muscle StO2 characteristics. In older individuals, working muscle tissue may reach lower oxygen saturation during exercise and take longer to return to baseline oxygen saturation post-exercise.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abe T, Thiebaud RS, Loenneke JP et al (2014) Association between forearm muscle thickness and age-related loss of skeletal muscle mass, handgrip and knee extension strength and walking performance in old men and women: a pilot study. Ultrasound Med Biol 40:2069–2075. https://doi.org/10.1016/j.ultrasmedbio.2014.05.003
Afaq A, Montgomery PS, Scott KJ et al (2008) The effect of hypercholestrolemia on calf muscle hemoglobin oxygen saturation in patients with intermittent claudication. Angiology 59:534–541. https://doi.org/10.1177/0003319707308728
Akazawa N, Okawa N, Tamura K, Moriyama H (2017) Relationships between intramuscular fat, muscle strength and gait independence in older women: a cross-sectional study. Geriatr Gerontol Int 17:1683–1688. https://doi.org/10.1111/ggi.12869
ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories (2002) ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med 166:111–117. https://doi.org/10.1164/ajrccm.166.1.at1102
Bauer TA, Brass EP, Hiatt WR (2004) Impaired muscle oxygen use at onset of exercise in peripheral arterial disease. J Vasc Surg 40:488–493. https://doi.org/10.1016/j.jvs.2004.06.025
Belardinelli R, Barstow TJ, Porszasz J, Wasserman K (1995) Changes in skeletal muscle oxygenation during incremental exercise measured with near infrared spectroscopy. Eur J Appl Physiol 70:487–492. https://doi.org/10.1007/BF00634377
Bhambhani YN (2004) Muscle oxygenation trends during dynamic exercise measured by near infrared spectroscopy. Can J Appl Physiol 29:504–523
Boas DA, Elwell CE, Ferrari M, Taga G (2014) Twenty years of functional near-infrared spectroscopy: introduction for the special issue. Neuroimage 85:1–5. https://doi.org/10.1016/j.neuroimage.2013.11.033
Bopp CM, Townsend DK, Barstow TJ (2011) Characterizing near-infrared spectroscopy responses to forearm post-occlusive reactive hyperemia in healthy subjects. Eur J Appl Physiol 111:2753–2761. https://doi.org/10.1007/s00421-011-1898-z
Bopp CM, Townsend DK, Warren S, Barstow TJ (2014) Relationship between brachial artery blood flow and total [hemoglobin+myoglobin] during post-occlusive reactive hyperemia. Microvasc Res 91:37–43. https://doi.org/10.1016/j.mvr.2013.10.004
Brocca L, McPhee JS, Longa E et al (2017) Structure and function of human muscle fibres and muscle proteome in physically active older men. J Physiol 595:4823–4844. https://doi.org/10.1113/JP274148
Burton K, Johnson P (1972) Reactive hyperemia in individual capillaries of skeletal muscle. Am J Physiol-Leg Content 223:517–524. https://doi.org/10.1152/ajplegacy.1972.223.3.517
Chambers TL, Burnett TR, Raue U et al (2020) Skeletal muscle size, function, and adiposity with lifelong aerobic exercise. J Appl Physiol 128:368–378. https://doi.org/10.1152/japplphysiol.00426.2019
Chung J, Ji S-H, Jang Y-E et al (2020) Evaluation of different near-infrared spectroscopy devices for assessing tissue oxygenation with a vascular occlusion test in healthy volunteers. J Vasc Res 57:341–347. https://doi.org/10.1159/000510072
Comerota AJ, Throm RC, Kelly P, Jaff M (2003) Tissue (muscle) oxygen saturation (StO2): a new measure of symptomatic lower-extremity arterial disease. J Vasc Surg 38:724–729. https://doi.org/10.1016/S0741-5214(03)01032-2
Crum EM, O’Connor WJ, Van Loo L et al (2017) Validity and reliability of the Moxy oxygen monitor during incremental cycling exercise. Eur J Sport Sci 17:1037–1043. https://doi.org/10.1080/17461391.2017.1330899
Cruz-Jentoft AJ, Baeyens JP, Bauer JM et al (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing 39:412–423. https://doi.org/10.1093/ageing/afq034
D’Antona G, Pellegrino MA, Carlizzi CN, Bottinelli R (2007) Deterioration of contractile properties of muscle fibres in elderly subjects is modulated by the level of physical activity. Eur J Appl Physiol 100:603–611. https://doi.org/10.1007/s00421-007-0402-2
De Blasi R, Luciani R, Punzo G et al (2009) Microcirculatory changes and skeletal muscle oxygenation measured at rest by non-infrared spectroscopy in patients with and without diabetes undergoing haemodialysis. Crit Care 13:S9. https://doi.org/10.1186/cc8007
Evans JM, Ziegler MG, Patwardhan AR et al (2001) Gender differences in autonomic cardiovascular regulation: spectral, hormonal, and hemodynamic indexes. J Appl Physiol 91:2611–2618. https://doi.org/10.1152/jappl.2001.91.6.2611
Fellahi J-L, Butin G, Zamparini G et al (2014) Lower limb peripheral NIRS parameters during a vascular occlusion test: an experimental study in healthy volunteers. Ann Fr Anesth Réanimation 33:e9–e14. https://doi.org/10.1016/j.annfar.2013.11.014
Fu T, Wang C, Lin P et al (2013) Aerobic interval training improves oxygen uptake efficiency by enhancing cerebral and muscular hemodynamics in patients with heart failure. Int J Cardiol 167:41–50. https://doi.org/10.1016/j.ijcard.2011.11.086
Fuglestad MA, Hernandez H, Gao Y et al (2020) A low-cost, wireless near-infrared spectroscopy device detects the presence of lower extremity atherosclerosis as measured by computed tomographic angiography and characterizes walking impairment in peripheral artery disease. J Vasc Surg 71:946. https://doi.org/10.1016/j.jvs.2019.04.493
Gardner AW, Skinner J, Cantwell B, Smith L (1991) Progressive vs single-stage treadmill tests for evaluation of claudication. Med Sci Sports Exerc 23:402–408
Gardner AW, Parker DE, Montgomery PS et al (2009) Sex differences in calf muscle hemoglobin oxygen saturation in patients with intermittent claudication. J Vasc Surg 50:77–82. https://doi.org/10.1016/j.jvs.2008.12.065
Gardner AW, Montgomery PS, Wang M, Shen B (2020) Association between calf muscle oxygen saturation with ambulatory function and quality of life in symptomatic patients with peripheral artery disease. J Vasc Surg 72:632–642. https://doi.org/10.1016/j.jvs.2019.09.057
Greig C, Butler F, Skelton D et al (1993) Treadmill walking in old age may not reproduce the real life situation. J Am Geriatr Soc 41:15–18. https://doi.org/10.1111/j.1532-5415.1993.tb05941.x
Gries KJ, Raue U, Perkins RK et al (2018) Cardiovascular and skeletal muscle health with lifelong exercise. J Appl Physiol 125:1636–1645. https://doi.org/10.1152/japplphysiol.00174.2018
Haykowsky MJ, Kouba EJ, Brubaker PH et al (2014) Skeletal muscle composition and its relation to exercise intolerance in older patients with heart failure and preserved ejection fraction. Am J Cardiol 113:1211–1216. https://doi.org/10.1016/j.amjcard.2013.12.031
Hirai DM, Craig JC, Colburn TD et al (2019) Skeletal muscle interstitial P o 2 kinetics during recovery from contractions. J Appl Physiol 127:930–939. https://doi.org/10.1152/japplphysiol.00297.2019
Ichimura S, Murase N, Osada T et al (2006) Age and activity status affect muscle reoxygenation time after maximal cycling exercise. Med Sci Sports Exerc 38:1277–1281. https://doi.org/10.1249/01.mss.0000227312.08599.f1
Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol Bethesda Md 1985(89):81–88. https://doi.org/10.1152/jappl.2000.89.1.81
Joyner MJ, Casey DP (2015) Regulation of increased blood flow (hyperemia) to muscles during exercise: a hierarchy of competing physiological needs. Physiol Rev 95:549–601. https://doi.org/10.1152/physrev.00035.2013
Kitzman DW, Nicklas B, Kraus WE et al (2014) Skeletal muscle abnormalities and exercise intolerance in older patients with heart failure and preserved ejection fraction. Am J Physiol-Heart Circ Physiol 306:H1364–H1370. https://doi.org/10.1152/ajpheart.00004.2014
Laughlin MH, Davis MJ, Secher NH et al (2012) Peripheral Circulation. In: Terjung R (ed) Comprehensive Physiology. John Wiley & Sons Inc, Hoboken, NJ, USA, pp 321–447
Maltepe E, Saugstad OD (2009) Oxygen in health and disease: regulation of oxygen homeostasis-clinical implications. Pediatr Res 65:261–268. https://doi.org/10.1203/PDR.0b013e31818fc83f
Mesquida J, Gruartmoner G, Espinal C (2013) Skeletal muscle oxygen saturation (StO 2) measured by near-infrared spectroscopy in the critically ill patients. BioMed Res Int 2013:1–8. https://doi.org/10.1155/2013/502194
Metter EJ, Lynch N, Conwit R et al (1999) Muscle quality and age: cross-sectional and longitudinal comparisons. J Gerontol Ser A 54:B207–B218. https://doi.org/10.1093/gerona/54.5.B207
Moreau KL, Donato AJ, Tanaka H et al (2003) Basal leg blood flow in healthy women is related to age and hormone replacement therapy status. J Physiol 547:309–316. https://doi.org/10.1111/j.2002.00309.x
Pandey A, Shah SJ, Butler J et al (2021) Exercise intolerance in older adults with heart failure with preserved ejection fraction. J Am Coll Cardiol 78:1166–1187. https://doi.org/10.1016/j.jacc.2021.07.014
Poole DC, Jones AM (2012) Oxygen Uptake Kinetics. In: Terjung R (ed) Comprehensive Physiology. John Wiley & Sons Inc, Hoboken, NJ, USA, p c100072
Quaresima V, Homma S, Azuma K et al (2001) Calf and shin muscle oxygenation patterns and femoral artery blood flow during dynamic plantar flexion exercise in humans. Eur J Appl Physiol 84:387–394. https://doi.org/10.1007/s004210100390
Quaresima V, Komiyama T, Ferrari M (2002) Differences in oxygen re-saturation of thigh and calf muscles after two treadmill stress tests. Comp Biochem Physiol A Mol Integr Physiol 132:67–73. https://doi.org/10.1016/S1095-6433(01)00531-1
Rantanen T, Volpato S, Luigi Ferrucci M et al (2003) Handgrip strength and cause-specific and total mortality in older disabled women: exploring the mechanism. J Am Geriatr Soc 51:636–641. https://doi.org/10.1034/j.1600-0579.2003.00207.x
Roberts H, Denison H, Martin H et al (2011) A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach. Age Ageing 40:423–429
Rosenberry R, Munson M, Chung S et al (2018) Age-related microvascular dysfunction: novel insight from near-infrared spectroscopy. Exp Physiol 103:190–200. https://doi.org/10.1113/EP086639
Saltin B, Rådegran G, Koskolou MD, Roach RC (1998) Skeletal muscle blood flow in humans and its regulation during exercise. Acta Physiol Scand 162:421–436. https://doi.org/10.1046/j.1365-201X.1998.0293e.x
Sousa-Santos AR, Amaral TF (2017) Differences in handgrip strength protocols to identify sarcopenia and frailty - a systematic review. BMC Geriatr 17:238. https://doi.org/10.1186/s12877-017-0625-y
Vardi M, Nini A (2008) Near-infrared spectroscopy for evaluation of peripheral vascular disease. a systematic review of literature. Eur J Vasc Endovasc Surg 35:68–74. https://doi.org/10.1016/j.ejvs.2007.07.015
Wilburn D, Ismaeel A, Machek S et al (2021) Shared and distinct mechanisms of skeletal muscle atrophy: a narrative review. Ageing Res Rev 71:101463. https://doi.org/10.1016/j.arr.2021.101463
Wray DW, Nishiyama SK, Harris RA et al (2012) Acute reversal of endothelial dysfunction in the elderly after antioxidant consumption. Hypertension 59:818–824. https://doi.org/10.1161/HYPERTENSIONAHA.111.189456
Yamaki T, Konoeda H, Osada A et al (2013) Measurements of calf muscle oxygenation during standing and exercise in patients with primary valvular insufficiency. J Vasc Surg Venous Lymphat Disord 1:333–340. https://doi.org/10.1016/j.jvsv.2013.05.002
Zoladz JA, Semik D, Zawadowska B et al (2005) Capillary density and capillary-to-fibre ratio in vastus lateralis muscle of untrained and trained men. Folia Histochem Cytobiol 43:11–17
Funding
This work was supported by the National Institute on Aging at the National Institutes of Health (USA) under grant number R01AG064420 to PK. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Author information
Authors and Affiliations
Contributions
MH: conceptualization, data curation, investigation, methodology, writing-original draft, PK: conceptualization, funding acquisition, project administration, resources, validation, writing-review and editing, AI: conceptualization, data curation, formal analysis, investigation, methodology, validation, visualization, writing-review and editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the Institutional Review Board at Baylor University (1081326).
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Communicated by I. Mark Olfert.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Holmes, M., Koutakis, P. & Ismaeel, A. Aging alters gastrocnemius muscle hemoglobin oxygen saturation (StO2) characteristics in healthy individuals. Eur J Appl Physiol 122, 1509–1520 (2022). https://doi.org/10.1007/s00421-022-04944-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-022-04944-0