The increase in maximal oxygen consumption (VO2max) with endurance training is associated with that of maximal cardiac output (Qmax), but not oxygen extraction, in young individuals. Whether such a relationship is altered with ageing remains unclear. Therefore, we sought systematically to review and determine the effect of endurance training on and the associations among VO2max, Qmax and arteriovenous oxygen difference at maximal exercise (Ca-vO2max) in healthy aged individuals.
Design and methods
We conducted a systematic search of MEDLINE, Scopus and Web of Science, from their inceptions until May 2015 for articles assessing the effect of endurance training lasting 3 weeks or longer on VO2max and Qmax and/or Ca-vO2max in healthy middle-aged and/or older individuals (mean age ≥40 years). Meta-analyses were performed to determine the standardised mean difference (SMD) in VO2max, Qmax and Ca-vO2max between post and pre-training measurements. Subgroup and meta-regression analyses were used to evaluate the associations among SMDs and potential moderating factors.
Results
Sixteen studies were included after systematic review, comprising a total of 153 primarily untrained healthy middle-aged and older subjects (mean age 42–71 years). Endurance training programmes ranged from 8 to 52 weeks of duration. After data pooling, VO2max (SMD 0.89; P < 0.0001) and Qmax (SMD 0.61; P < 0.0001) were increased after endurance training; no heterogeneity among studies was detected. Ca-vO2max was only increased with endurance training interventions lasting more than 12 weeks (SMD 0.62; P = 0.001). In meta-regression, the SMD in Qmax was positively associated with the SMD in VO2max (B = 0.79, P = 0.04). The SMD in Ca-vO2max was not associated with the SMD in VO2max (B = 0.09, P = 0.84).
Conclusions
The improvement in VO2max following endurance training is a linear function of Qmax, but not Ca-vO2max, through healthy ageing.
BeerePARussellSDMoreyMC. Aerobic exercise training can reverse age-related peripheral circulatory changes in healthy older men. Circulation1999; 100: 1085–1094.
2.
EhsaniAAOgawaTMillerTR. Exercise training improves left ventricular systolic function in older men. Circulation1991; 83: 96–103.
3.
FujimotoNPrasadAHastingsJL. Cardiovascular effects of 1 year of progressive and vigorous exercise training in previously sedentary individuals older than 65 years of age. Circulation2010; 122: 1797–1805.
4.
HaennelRTeoKKQuinneyA. Effects of hydraulic circuit training on cardiovascular function. Med Sci Sports Exerc1989; 21: 605–612.
5.
HijaziOMRamanathanMEstreraAS. Fixed maximal stroke index in patients after pneumonectomy. Am J Respir Crit Care Med1998; 157: 1623–1629.
6.
MarshallPAl-TimmanJRileyR. Randomized controlled trial of home-based exercise training to evaluate cardiac functional gains. Clin Sci2001; 101: 477–483.
7.
McGuireDKLevineBDWilliamsonJW. A 30-year follow-up of the Dallas bedrest and training study: II. Effect of age on cardiovascular adaptation to exercise training. Circulation2001; 104: 1358–1366.
8.
MorrisNGassGThompsonM. Rate and amplitude of adaptation to intermittent and continuous exercise in older men. Med Sci Sports Exerc2002; 34: 471–477.
9.
MuriasJMKowalchukJMPatersonDH. Time course and mechanisms of adaptations in cardiorespiratory fitness with endurance training in older and young men. J Appl Physiol (1985)2010; 108: 621–627.
10.
MuriasJMKowalchukJMPatersonDH. Mechanisms for increases in VO2max with endurance training in older and young women. Med Sci Sports Exerc2010; 42: 1891–1898.
11.
SpinaRJOgawaTKohrtWM. Differences in cardiovascular adaptations to endurance exercise training between older men and women. J Appl Physiol (1985)1993; 75: 849–855.
12.
SpinaRJOgawaTMillerTR. Effect of exercise training on left ventricular performance in older women free of cardiopulmonary disease. Am J Cardiol1993; 71: 99–104.
13.
SpinaRJTurnerMJEhsaniAA. Beta-adrenergic-mediated improvement in left ventricular function by exercise training in older men. Am J Physiol-Heart Circulat Physiol1998; 274: H397–H404.
14.
WangENæssMSHoffJ. Exercise-training-induced changes in metabolic capacity with age: The role of central cardiovascular plasticity. Age2014; 36: 665–676.
15.
Huang G, Wang R, Chen P, et al. Dose–response relationship of cardiorespiratory fitness adaptation to controlled endurance training in sedentary older adults. Eur J Prev Cardiol 2015. Epub ahead of print 21 April 2015. DOI: 10.1177/2047487315582322.
16.
BaggishALWangFWeinerRB. Training-specific changes in cardiac structure and function: A prospective and longitudinal assessment of competitive athletes. J Appl Physiol (1985)2008; 104: 1121–1128.
17.
SealsDRHagbergJMSpinaRJ. Enhanced left ventricular performance in endurance trained older men. Circulation1994; 89: 198–205.
18.
SawkaMNConvertinoVAEichnerER. Blood volume: Importance and adaptations to exercise training, environmental stresses, and trauma/sickness. Med Sci Sports Exerc2000; 32: 332–348.
19.
HagbergJMGoldbergAPLakattaL. Expanded blood volumes contribute to the increased cardiovascular performance of endurance-trained older men. J Appl Physiol (1985)1998; 85: 484–489.
20.
BonneTCDoucendeGFluckD. Phlebotomy eliminates the maximal cardiac output response to six weeks of exercise training. Am J Physiol Regul Integr Comp Physiol2014; 306: R752–760.
21.
MuriasJMKowalchukJMRitchieD. Adaptations in capillarization and citrate synthase activity in response to endurance training in older and young men. J Gerontol A Biol Sci Med Sci2011; 66: 957–964.
22.
GrimbyGSaltinB. The ageing muscle. Clin Physiol1983; 3: 209–218.
23.
HoppelerHHowaldHConleyK. Endurance training in humans: Aerobic capacity and structure of skeletal muscle. J Appl Physiol (1985)1985; 59: 320–327.
24.
JacobsRAFluckDBonneTC. Improvements in exercise performance with high-intensity interval training coincide with an increase in skeletal muscle mitochondrial content and function. J Appl Physiol (1985)2013; 115: 785–793.
25.
JacobsRALundbyC. Mitochondria express enhanced quality as well as quantity in association with aerobic fitness across recreationally active individuals up to elite athletes. J Appl Physiol (1985)2013; 114: 344–350.
26.
KlausenKSecherNHClausenJP. Central and regional circulatory adaptations to one-leg training. J Appl Physiol Respir Environ Exerc Physiol1982; 52: 976–983.
27.
WengTPHuangSCChuangYF. Effects of interval and continuous exercise training on cd4 lymphocyte apoptotic and autophagic responses to hypoxic stress in sedentary men. PLoS One2013; 8: e80248–e80248.
28.
MakridesLHeigenhauserGJJonesNL. High-intensity endurance training in 20- to 30- and 60- to 70-yr-old healthy men. J Appl Physiol (1985)1990; 69: 1792–1798.
29.
KalliokoskiKKOikonenVTakalaTO. Enhanced oxygen extraction and reduced flow heterogeneity in exercising muscle in endurance-trained men. Am J Physiol Endocrinol Metab2001; 280: E1015–1021.
30.
EkblomBAstrandPOSaltinB. Effect of training on circulatory response to exercise. J Appl Physiol1968; 24: 518–528.
31.
SaltinBBlomqvistGMitchellJH. Response to exercise after bed rest and after training. Circulation1968; 38: VII1–78.
32.
SaltinBCalbetJA. Point: In health and in a normoxic environment, VO2max is limited primarily by cardiac output and locomotor muscle blood flow. J Appl Physiol (1985)2006; 100: 744–745.
33.
Arbab-ZadehAPerhonenMHowdenE. Cardiac remodeling in response to 1 year of intensive endurance training. Circulation2014; 130: 2152–2161.
34.
Montero D, Diaz-Canestro C and Lundby C. Endurance training and VO2max: Role of maximal cardiac output and oxygen extraction. Med Sci Sports Exerc 2015; 47: 2024--2033.
35.
OgawaTSpinaRJMartinWHIII. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation1992; 86: 494–503.
36.
RoltschMHBrownMDHandBD. No association between ace i/d polymorphism and cardiovascular hemodynamics during exercise in young women. Int J Sports Med2005; 26: 638–644.
37.
Carrick-RansonGHastingsJLBhellaPS. The effect of lifelong exercise dose on cardiovascular function during exercise. J Appl Physiol2014; 116: 736–745.
38.
FlegJLSchulmanSPO’ConnorFC. Cardiovascular responses to exhaustive upright cycle exercise in highly trained older men. J Appl Physiol1994; 77: 1500–1506.
39.
StroupDFBerlinJAMortonSC. Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA2000; 283: 2008–2012.
40.
Marinho VC, Higgins JP, Sheiham A, et al. Fluoride toothpastes for preventing dental caries in children and adolescents. Cochrane Database Syst Rev 2003: CD002278.
41.
RossLEGrigoriadisSMamisashviliL. Quality assessment of observational studies in psychiatry: An example from perinatal psychiatric research. Int J Methods Psychiatr Res2011; 20: 224–234.
42.
MonteroDPadillaJDiaz-CanestroC. Flow-mediated dilation in athletes: Influence of aging. Med Sci Sports Exerc2014; 46: 2148–2158.
43.
SprungVSAtkinsonGCuthbertsonDJ. Endothelial function measured using flow-mediated dilation in polycystic ovary syndrome: A meta-analysis of the observational studies. Clin Endocrinol (Oxford)2013; 78: 438–446.
44.
Higgins JPT and Green S (eds). Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. www.Cochrane-handbook.Org (2011, accessed 25 August 2013).
45.
DerSimonianRLairdN. Meta-analysis in clinical trials. Control Clin Trials1986; 7: 177–188.
46.
EggerMDavey SmithGSchneiderM. Bias in meta-analysis detected by a simple, graphical test. BMJ1997; 315: 629–634.
47.
ACSM. ACSM’s guidelines for exercise testing and prescription. Baltimore, Maryland, USA: Lippincott Raven, 2009.
48.
IoannidisJP. Why most published research findings are false. PLoS Med2005; 2: e124–e124.
49.
Montero D, Walther G, Diaz-Canestro C, et al. Microvascular dilator function in athletes: A systematic review and meta-analysis. Med Sci Sports Exerc 2014; 47: 1485--1494.
50.
MonteroD. The association of cardiorespiratory fitness with endothelial or smooth muscle vasodilator function. Eur J Prev Cardiol2015; 22: 1200–1211.
51.
Lundby C and Montero D. Diffusion limitation of O2 from microvessels in to muscle does not contribute to the limitation of VO2max. J Physiol 2015; 22: 1200--1211.
52.
GleserMA. Effects of hypoxia and physical training on hemodynamic adjustments to one-legged exercise. J Appl Physiol1973; 34: 655–659.
53.
CalbetJARadegranGBoushelR. On the mechanisms that limit oxygen uptake during exercise in acute and chronic hypoxia: Role of muscle mass. J Physiol2009; 587: 477–490.
54.
DaussinFNPonsotEDufourSP. Improvement of VO2max by cardiac output and oxygen extraction adaptation during intermittent versus continuous endurance training. Eur J Appl Physiol2007; 101: 377–383.
55.
NgAVCallisterRJohnsonDG. Endurance exercise training is associated with elevated basal sympathetic nerve activity in healthy older humans. J Appl Physiol (1985)1994; 77: 1366–1374.
56.
DaussinFNZollJDufourSP. Effect of interval versus continuous training on cardiorespiratory and mitochondrial functions: Relationship to aerobic performance improvements in sedentary subjects. Am J Physiol Regul Integr Comp Physiol2008; 295: R264–272.
57.
BakerWLWhiteCMCappelleriJC. Understanding heterogeneity in meta-analysis: The role of meta-regression. Int J Clin Pract2009; 63: 1426–1434.
58.
RossRM. ATS/ACCP statement on cardiopulmonary exercise testing. Am J Respir Crit Care Med2003; 167: 1451–1451. author reply 1451.
59.
WarburtonDEHaykowskyMJQuinneyHA. Reliability and validity of measures of cardiac output during incremental to maximal aerobic exercise. Part I: Conventional techniques. Sports Med1999; 27: 23–41.
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