Introduction Heart rate variability (HRV), blood pressure variability (BPV) and baroreceptor sensitivity (BRS) are often used as measures of auto- nomic activity, even though reported results are not always compa- rable or as expected. It is known that endurance athletes have lower average resting heart rates than non-exercising individuals. 33, 50 However, other exercise-induced autonomic influences on cardiac control are far more controversial. Autonomic control via sympathetic and parasympathetic modulation of the heart has been assessed by power spectral analysis of HRV 1,7,33,41,46,48,50 and BPV. 44,52 Different frequency peaks reflect specific physiological stimuli and it is possible to estimate the involvement of the autonomic nervous system (ANS) influence and balance in heart rate (HR) regulation. 1,2,6 With power spectral analysis of HR, two characteristic peaks between 0.04 Hz and 0.15 Hz (A) and between 0.15 Hz and 0.5 Hz (B) are used to quantify the autonomic balance in terms of the low-frequency (LF)/ high-frequency (HF) ratio. 1,6,48 Peak A is found in the region of Mayer waves (0.1 Hz) and is situated in the so-called LF area. It appears to be linked to the combined activities of the sympathetic and parasympathetic branches of the ANS. Peak B is synchronous with respiration, reflects vagal activity, is situated in the so-called HF area REVIEW Autonomic response to exercise as measured by cardio- vascular variability Abstract Motivation. There is growing interest in the use of cardiovas- cular variability indicators as measures of autonomic activity, even though reported results are not always comparable or as expected. This review aims to determine the consistency of re- sults reported on the autonomic response to physical exercise as measured by heart rate variability, blood pressure variability and baroreceptor sensitivity. Method. An Ovid MEDLINE Database search for the period 1950 - March 2008 produced 46 articles for review. The published arti- cles that evaluate the effect of exercise on the autonomic nervous system (ANS) are summarised in three categories: the response of the ANS during a bout of exercise, directly after exercise (recov- ery measurements), and after a long-term exercise programme. Results. Articles on the effect of training on the ANS as measured by cardiovascular variability indicators show increased variability, decreased variability, and no change in variability. Conclusion. Findings in this review emphasise that standardisa- tion and refinement of these measuring tools are essential to pro- duce results that can be repeated and used as reference. Stand- ardisation is essential as these measurements are increasingly employed in studies regarding investigations of central autonomic regulation, those exploring the link between psychological pro cesses and physiological functioning, and those indicating ANS activity in response to exercise, training and overtraining. This review shows that important aspects are inter-individual differenc- es, duration and intensity of the exercise programme, and choice and specific implementation of variability analysis techniques. CoRREspondEnCE: Mrs C C Grant Section Sports Medicine University of Pretoria Tel: 27 12 3624496 Fax: 27 12 3623369 E-mail: Rina.Grant@up.ac.za C C Grant (Msc)1 J A Ker (MB ChB, MMed (Int), Md)2 1Section Sports Medicine, University of Pretoria 2Department of Internal Medicine, University of Pretoria 102 sAJsM Vol 20 no. 4 2008 Fig. 1. Summary of the Ovid MEDLINE Database search. Autonomic nervous system (physiology) Baroreflex (physiology) Exercise 27118 articles 2084 articles 38434 articles 463 articles OR AND Exclude: not English not human 340 articles Select studies using HRV, BPV and BRS as ANS indicators 46 articles Fig. 1. Summary of the Ovid MEDLINE Database search. and also gives an indication of respiratory sinus arrhythmia (RSA). 1,48 During measurement of systolic BPV the LF peak corresponds with sympathetic activity while the HF peak is determined by mechanical effects of respiration on intrathoracic pressure and cardiac filling. 44,52 The variability in blood pressure and identification of the corresponding physiological stimuli are difficult to identify. Indications are that the very low frequencies (≤0.04 Hz) are influenced by vascular tone, endothelium factors and thermoregulation, and the LF peak (0.07 - 0.15 Hz) relates to sympathetic activity and represents vasomotor tone. 2 BRS reflects mainly vagal modulation of the HR by the arterial baroreceptors and the magnitude of response in heart beat interval to a change in blood pressure (ms/mmHg). 6 Physical exercise requires rapid and complex physiological adaptation, particularly by the ANS. Exercise programmes require changes in the neural cardiovascular and ANS control that are unique to the person and his/her surroundings. This review aims to determine the consistency of results reported on the autonomic response to physical exercise as measured by HRV, BPV and BRS. Method An Ovid MEDLINE Database search was conducted for the period 1950 - March 2008 (Fig. 1). The term ‘ANS (physiology)’ produced 27 118 articles, and ‘baroreflex (physiology)’ 2 084 articles. When link- ing the results with the term ‘exercise’ (38 434 articles) and then limit- ing the results to ‘humans and English’, 340 references were found. Only articles that used HRV (determined by time-domain analysis, Poincaré analysis and/or frequency-domain analysis), non-invasive BPV and BRS as indicators of autonomic function were selected, yielding 46 articles. Results Published articles on the effect of exercise on the ANS as measured by HRV and BPV are summarised in three categories: the response of the ANS measured during a bout of exercise, 3,5,14,16,26,29,37,42,43,51 and directly after a bout of exercise (recovery measurements), 3,9,22- 24,28,40,49 and the long-term effect of regular exercise on the ANS. 4,8,10-13,15,17,18,19-21,25,27,30-32,34-36,38,39,45,47 The results of 10 articles on ANS response measured during exercise are shown in Table I. Some authors expressed concern about the measurement of spectral analysis of HRV during exercise, while others reported increases (↑), decreases (↓) and no changes in variability indicators (↔) of sympathetic (SNS) and parasympathetic (PNS) influence. Table II shows results of 10 articles on the response of the ANS measured after a bout of exercise (recovery measurements). Comments found were based on time domain, spectral and coarse- sAJsM Vol 20 no. 4 2008 103 TABlE I. Articles on the response of the Ans measured during a bout of exercise Reference number Author/s Title Cardiovascular variability indicator 43 Sandercock et al. The use of HRV measures to Results from spectral analysis assess autonomic control of HRV not as expected; more during exercise research needed: word of caution 5 Banach et al. HRV during incremental cycling Spectral and time domain exercise in healthy, untrained analysis of HRV young men ↓SDNN, RMSSD ↓LF, HF; LF/HF ↓Ptot 16 Freeman et al. ANS interaction with the CV Encourage the use of HRV at system during exercise rest and during exercise 14 Eryonucu et al. The effect of ANS activity on Used spectral analysis of HRV in a exaggerated blood pressure comparative study response to exercise: evaluation by HRV 29 Lucini et al. Analysis of initial autonomic Spectral analysis of HRV adjustments to moderate ↑LF suggest ↑SNS exercise in humans ↓HF suggest ↓PNS ↔ and ↑LF of BPV 42 Saito and Nakamura Cardiac autonomic control and Spectral analysis of HRV muscle sympathetic nerve ↓LF power, ↓ HF power, activity during dynamic exercise ↔total power ↑LF/HF: SNS↑ ↓HF/Ptot : PNS↓ 26 Kamath et al. Effects of steady-state exercise Spectral analysis of HRV on the power spectrum of HRV ↓LF,↓HF, SNS↓, PNS↓ 3 Arai et al. Modulation of cardiac autonomic Spectral analysis of HRV activity during and immediately ↓HF after exercise ↓LF 51 Yamamoto et al. Autonomic control of HR during Spectral analysis of HRV exercise studied by HRV ↓HF: PNS↓ spectral analysis ↑and↔LF/HF:↑ and ↔SNS 37 Perini and Veicsteinas HRV and autonomic activity at rest Spectral analysis of HRV and during exercise in various No change in HF and LF physiological conditions power during increased loads ↔HF, ↔LF LF = low frequency; HFR = high frequency; SDN = standard deviation of all intervals; Ptot = total frequency power; pNN50 = percentage of successive interval differences greater than 50ms; SNS = sympathetic nervous system; PNS = parasympathetic nervous system; SAP = systolic arterial pressure. graining analysis of HRV and BRS via the sequence technique and spectral analysis of BPV. Table III summarises findings on the long-term effect of regular exercise on the ANS. Some of the different techniques used to estimate cardiovascular variability were time domain and spectral analysis of HRV, BRS via sequence technique and the alpha index, spectral analysis of BRS and also BRS via the slope of the baroreflex sequences and transfer function gain. discussion Articles published on cardiovascular variability measured during ex- ercise concluded that the interpretation of variability measurements is difficult because indicators reflecting sympathovagal interactions at rest do not behave as expected during exercise and that the in- creased respiratory effort had a confounding effect on HF bands. 43 It is also suggested that the presence of cross-sectional differences between HRV in athletes and non-athletes should be noted and that one should not use HRV data to determine autonomic control during exercise. Doubt was expressed on the applicability of the HRV pow- er-spectrum analysis, with its present interpretation, to assess the sympathovagal interaction during exercise. 5 However, other authors encouraged the use of HRV components at rest and during exercise as prognostic indicators, but called for the refinement of exercise measurements. 16 Eryonucu et al. used HRV as an indicator of ANS activity before, during and after exercise in a comparative study. 14 Two other studies reported increased sympathetic influence (meas- ured by LF and LF/HF) on autonomic cardiac control during graded exercise, 29,42 including increased, peripheral, vascular sympathetic activation at 30% of maximum exercise in the study by Saito and Na- kamura. 42 These results were in direct conflict with studies indicat- ing significant suppression of both SNS and PNS autonomic cardiac control during graded exercise measured by the LF and HF of the power spectrum of HRV. 3,26 In 1991 Yamamoto et al. 51 reported de- creased PNS activity (HF) and unchanged SNS activity (LF/HF) up to 100% of the predetermined ventilatory threshold (Tvent), with an abrupt increase in SNS activity (LF/HF) only at 100% Tvent. Perini and Veicsteinas 37 concluded that changes in HF and LF power and in LF/HF observed during exercise do not reflect the decrease in vagal activity and the activation of the SNS at increasing loads; nei- ther did fitness level, age and hypoxia have any influence. However, exercising at medium-high intensities in the supine position did pro- duce measurable increased power in LF. Cardiovascular variability measured during recovery from a single bout of endurance exercise indicated that the total power of HRV 104 sAJsM Vol 20 no. 4 2008 TABlE II. Articles on the response of the Ans measured directly after a bout of exercise (recovery measurements) Reference number Author/s Title Cardiovascular variability indicator 24 Heffernan et al. Cardiac autonomic modulation Spectral analysis of HRV during recovery from acute After endurance: endurance v. resistance exercise ↔total power, ↑LF/HF, After resistance: ↓total power of HRV, ↑LF/HF 49 Terziotti et al. Post-exercise recovery of autonomic Spectral analysis of HRV and BPV cardiovascular control: a study by ↑LF of systolic blood pressure spectrum and cross-spectrum analysis ↓HF activity of heart rate ↓decreased BRS in humans 22 Hayashi et al. Cardiac autonomic regulation after Coarse-graining spectral analysis of HRV moderate and exhaustive exercises ↓HF ↑LF/HF 40 Raczak et al. Cardiovagal response to acute Time domain and spectral analysis mild exercise in young healthy subjects of HRV and BRS ↑SDNN ↔LF and HF ↓BRS 26 Kamath et al. Effects of steady state exercise Spectral analysis of HRV on the power spectrum of HRV ↑LF activity 23 Heffernan Arterial stiffness and baroreflex BRS via the sequence technique sensitivity following bouts of aerobic ↓BRS after resistance and aerobic exercise. and resistance exercise Greater reduction after resistance 9 Brown and Brown Resting and post-exercise cardiac Time domain and spectral analysis of HRV autonomic control in trained ↓SDRR , ↓total power, ↓HF. master athletes ↔LF 28 Lucini et al. Selective reductions of cardiac Spectral analysis of HRV and BPV autonomic responses to light bicycle HRV decreases with age exercise with aging in healthy humans BRS via sequence technique 15 Figueroa et al. Endurance training improves Spectral analysis of HRV post-exercise cardiac autonomic BRS via sequence technique modulation in obese women ↑HF, LF, BRS with and without type 2 diabetes 3 Arai et al. Modulation of cardiac autonomic Spectral analysis of HRV activity during and immediately ↓HF, ↓LF after exercise LF = low frequency; HFR = high frequency; SDN = standard deviation of all intervals; Ptot = total frequency power; pNN50 = percentage of successive interval differences greater than 50ms; SNS = sympathetic nervous system; PNS = parasympathetic nervous system; SAP = systolic arterial pressure. SAJSM vol 19 No. 4 2007 105sAJsM Vol 20 no. 4 2008 105 TABlE III. Articles on the long-term autonomic effects of regular exercise Cardiovascular Reference number Author/s name variability indicator 15 Figueroa et al. Endurance training improves post-exercise Spectral analysis of HRV cardiac autonomic modulation in obese BRS via sequence technique women with and without type 2 diabetes ↔HRV and BRS: no baseline changes 47 Spierer et al. Exercise training improves cardiovascular Spectral analysis of HRV and autonomic profiles in HIV BRS via alpha index ↑BRS increased ↑HF ↓LF/HF 4 Aubert et al. Low-dose exercise does not influence Spectral analysis of HRV cardiac autonomic control in healthy ↔LF, HF, LF/HF sedentary men aged 55 - 75 years 31 Martinelli et al. HRV in athletes and non-athletes at Spectral analysis of HRV rest and during head-up tilt ↑SDNN ↔LF, HF: SNS/PNS↔ 45 Sharma et al. Short term physical training alters Time domain and spectral cardiovascular autonomic response analysis of HRV amplitude and latencies ↔HRV indicators 37 Perini and HRV and autonomic activity at rest and Spectral analysis of HRV Veicsteinas during exercise in various physiological Fitness level has no influence conditions 10 Buchheit and Cardiac parasympathetic regulation: Time domain and spectral Gindre respective associations with cardiorespiratory analysis of HRV fitness and training load ↑HF, RMSSD, PNN50 39 Raczak et al. Long-term exercise training improves Time domain and spectral analysis ANS profile in professional runners of HRV, spectral analysis of BRS ↑SDNN, pNN50, RMSSD, ↑Total power and LF ↑BRS 36 Okazaki et al. Dose-response relationship of endurance Spectral analysis of HRV training for autonomic circulatory control BRS via transfer function gain in healthy seniors ↑SDRR, LF, HF ↑BRS 32 Melo et al. Effects of age and physical activity on Time domain and spectral the autonomic control of heart rate in analysis of HRV healthy men ↑RMSSD ↓HR 19 Goldsmith et al. Exercise and autonomic function Review ↑SNS activity ↓PNS activity 17 Goldsmith et al. Physical fitness as a determinant Spectral analysis of HRV of vagal modulation ↑HF 27 Kiviniemi et al. Cardiac vagal outflow after aerobic training Spectral analysis of HRV by analysis of high-frequeny oscillation ↑HF of the R-R interval 12 Cooke et al. Effects of training on CV and sympathetic Time domain analysis of HRV, BRS responses to Valsalva’s maneuver ↑SDRR ↑BRS 13 Costes et al. Influence of exercise training on BRS via the slope of the baroreflex cardiac BRS in patients with COPD sequences between systolic blood pressure changes ↑BRS 34 Monahan et al. Regular aerobic exercise modulates BRS via linear regression between age-associated declines in cardiovagal BP en RR intervals during baroreflex sensitivity in healthy men a Valsalva maneuver ↑BRS 11 Carter et al. Effect of endurance training on autonomic Review control of heart rate – review ↓SNS activity ↓PNS activity 25 Iellamo et al. Conversion from vagal to sympathetic Spectral analysis of HRV predominance with strenuous training BRS via the sequences method in high-performance athletes 100% training load reverse effects: ↑LF,↓HF, BRS↓ 8 Bowman et al. Effects of aerobic exercise training and BRS via the alpha index yoga on the baroreflex in healthy ↔BRS elderly persons did not alter compared with significantly reduced total power found after resistance exercise. However, the LF/HF ratio was significantly increased after both resistance and endurance exercise, indicating increased SNS (LF) and/or decreased PNS (HF) influence. 24 This corresponds with results published by Terziotti et al., who found a reduced HF (vagal) component of HR and decreased BRS during 15 minutes of recovery. 49 Another study 22 also found suppressed vagal (HF) activities 10 minutes of recovery after 100% of the individual ventilatory threshold compared with baseline values. Raczak et al. found no differences in HF and LF activities between pre- and post-exercise measurements, but increased BRS and overall HRV as measured by standard deviation of all intervals (SDNN) after exercise. 40 However, Kamath et al. 26 and Figueroa et al. 15 reported significant increased LF power during post-exercise recovery. This contrasts with findings by Arai et al., who reported significantly decreased HR power at all frequencies compared with baseline values in normal subjects. 3 Decreased BRS and HRV after exercise were also reported in other studies. 9,23 Lucini et al. reported that ageing progressively reduces the cardiac autonomic excitatory response to light exercise. 28 Articles on the effect of an endurance training programme over a period of time also showed a wide range of results. One study 15 reported no change in baseline BRS and HRV values after a 16- week fitness programme, while another found increased BRS when comparing fitness levels. 47 Aubert et al. also found no evidence of significant changes in resting autonomic modulation of the sinus node after a low-volume, moderate-intensity 1- year exercise programme. 4 Comparing 11 young sedentary participants and 10 endurance-trained cyclists Martinelli et al. found no difference in power-spectral components of HRV at rest. 31 However, a lower HR and higher values for time domain HRV indicators were reported during rest and head-up tilt, concluding that resting bradycardia seems to be more related to changes in intrinsic mechanisms than to ANS control modifications. Sharma et al. found no statistically significant changes in autonomic cardiovascular control measured by HRV after a physical training programme of 15 days. 45 Perini and Veicsteinas 37 reported no influence of factors such as age and fitness level, while Bucheit and Gindre 10 showed that modifications in autonomic activities induced by training are visible in HRV power spectra at rest. Rackzak et al. 39 reported PNS dominance by measuring HRV and increased BRS after long-term exercise training. Another study 36 reported increased HRV and BRS in Masters Athletes compared with decreased values for sedentary seniors. Several other studies also concluded that regular physical activity increases vagal influence on the HR and BRS, while the sympathetic tone may be decreased. 8,11-13,17,19,25,27,32,34 However, Iellamo et al. 25 found a reversal of these effects after a period of training at 100% training load. Very intensive training shifted the CV autonomic modulation from PNS toward SNS predominance. Increases were reported in all components of HRV after a 1-year exercise training programme in children who initially had low HRV. 35 In 2001 Pigozzi et al. 38 found that a 5-week exercise training period in female athletes increased the SNS cardiac modulation, which may coexist with relatively reduced or unaffected vagal modulation. Gulli et al. 20 reported increased LF reactivity (SNS) and BRS after a moderate aerobic training programme in older women. In 1992 Goldsmith et al. 18 noted that, although exercise training may increase PNS activity, studies report conflicting results. As seen from the above summary, nearly two decades later conflicting results persist when the effects of exercise training on the ANS is measured during exercise, directly after exercise and after a long-term exercise programme. Possible confounding factors mentioned and identified are listed in Table IV. A possible explanation for conflicting results is that the individual’s response is greatly influenced by the baseline cardiovascular autonomic function, thus producing large inter-subject variation in the 106 sAJsM Vol 20 no. 4 2008 TABlE III. Articles on the long-term autonomic effects of regular exercise – continued 35 Nagai et al. Moderate physical exercise increases Spectral analysis of HRV cardiac ANS activity in children with low HRV ↑LF, ↓HF 38 Pigozzi et al. Effects of aerobic exercise training on 24hr Time domain and spectral profile of HRV in female athletes analysis of HRV ↔Time domain ↔LF, HF (daytime) 20 Gulli et al. Moderate aerobic training improves Spectral analysis of HRV and BPV autonomic CV control in older women ↑BRS ↑LF (RR), LF (SAP) 18 Goldsmith et al. Comparison of 24-hour parasympathetic Report conflicting results activity in endurance-trained and Spectral analysis of HRV untrained young men ↑HF 21 Hautala et al. Cardiovascular autonomic function correlates Baseline vagal (HF) influences with the response to aerobic training in determines effect of exercise training healthy sedentary subjects LF = low frequency; HFR = high frequency; SDN = standard deviation of all intervals; Ptot = total frequency power; pNN50 = percentage of successive interval differences greater than 50ms; SNS = sympathetic nervous system; PNS = parasympathetic nervous system; SAP = systolic arterial pressure. TABlE IV. possible confounding factors Inter-individual variation Baseline cardiovascular autonomic function Age Gender Fitness BMI Diet Alcohol consumption Smoking Analysis techniques Time and frequency domain measures do not describe non-linear features in HR behaviour Use of DA, ApEn Length of sampling time (tachogram) Training/exercise Length of training period Intensity of training Type of exercise: resistance or endurance sAJsM Vol 20 no. 4 2008 107 conventional non-spectral and spectral measures of cardiovascular variability. Hautala et al. 21 suggested that high vagal activity at baseline is associated with improvement in aerobic power caused by aerobic exercise training. We also observed that some studies used non-homogeneous participant groups with regard to age, gender and BMI, while others did not include these in the participant description. Factors often not taken into consideration are baseline blood pressure, blood cholesterol and diet. The effect of duration and intensity of the training programme as well as the type of exercise (endurance or resistance) may have been underestimated in studies on the ANS and exercise. 24 In this review training periods from 15 days to 1 year were studied and the different degrees of exercise intensity used were not even mentioned in many articles. 22 The choice and specific analysis techniques implemented may also play a role in the observed conflicting results. The recommended sampling time (tachogram) for HRV analysis is 5 minutes, 48 but different time windows were selected by different authors – 5 minutes, 10 minutes, 15 minutes and 24 hours. The articles studied used mostly traditional measures of variability, such as time and frequency. However, it is known that non-linear phenomena are involved in cardiovascular control. Therefore, the use of analysis techniques that acknowledge this fact should be co-implemented and reported with traditional measures. Examples include the measurement of fractal scaling exponents (describes the fractal-like correlation properties of R-R interval data) and ApEn (quantifies the amount of complexity in the time series data). 30 Conclusions This review demonstrates the wide variety of results published during the past decades on the effect of training on the ANS as measured by cardiovascular variability indicators. It is clear from the results that standardisation and refinement of these measuring tools are essential to produce repeatable results that can be used as refer- ences in other studies. This is necessary as these measurements are increasingly employed in studies ranging from investigations of central autonomic regulation; to studies exploring the link between psychological processes and physiological functioning; to the indica- tion of ANS activity in response to exercise, training and overtraining. 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