Autonomic response to exercise as measured by cardio- vascular variability

Motivation. There is growing interest in the use of cardiovascular 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 results 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 articles 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 (recovery 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 standardisation and refinement of these measuring tools are essential to produce results that can be repeated and used as reference. Standardisation 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 differences, duration and intensity of the exercise programme, and choice and specific implementation of variability analysis techniques.


Introduction
Heart rate variability (HRV), blood pressure variability (BPV) and baroreceptor sensitivity (BRS) are often used as measures of autonomic activity, even though reported results are not always comparable 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. 44,52Different 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. 1,2,6With 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. 1,6,48Peak 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 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 limiting 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.
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 exercise 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 increased 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 power-spectrum analysis, with its present interpretation, to assess the sympathovagal interaction during exercise. 5However, other authors encouraged the use of HRV components at rest and during exercise as prognostic indicators, but called for the refinement of exercise measurements. 16Eryonucu et al. used HRV as an indicator of ANS activity before, during and after exercise in a comparative study.
Two other studies reported increased sympathetic influence (measured 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 Nakamura. 42These results were in direct conflict with studies indicating 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. 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. 24This 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. 49Another 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. 40However, 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. 3Decreased BRS and HRV after exercise were also reported in other studies.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 16week fitness programme, while another found increased BRS when comparing fitness levels. 47Aubert et al. also found no evidence of significant changes in resting autonomic modulation of the sinus node after a low-volume, moderate-intensity 1year exercise programme. 432,34 However, Iellamo et al. 25 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. 24In 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. 22The 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 references 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 indication of ANS activity in response to exercise, training and overtraining.Important aspects to consider when developing standardised procedures are inter-individual differences, duration and intensity of the exercise programme, and the choice and implementation of a specific variability analysis technique.Much more research needs to be done to fully describe and accurately quantify the effect of exercise on the ANS.

Fig. 1 .
Fig. 1.Summary of the Ovid MEDLINE Database search.

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-

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)
3,26In 1991 Yamamoto et al.

20 no. 4 2008 105 TABlE III. Articles on the long-term autonomic effects of regular exercise
Comparing 11 young sedentary participants and 10 endurance-trained cyclists Martinelli et al. found no difference in power-spectral components of HRV at rest.
31However, 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.

106 sAJsM Vol 20 no. 4 2008 TABlE III. Articles on the long-term autonomic effects of regular exercise -continued
= 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. LF