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Am J Physiol Heart Circ Physiol 285: H1747-H1752, 2003. First published June 19, 2003; doi:10.1152/ajpheart.00202.2003
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Cardiovascular autonomic function correlates with the response to aerobic training in healthy sedentary subjects

Arto J. Hautala,1,2 Timo H. Mäkikallio,1,2 Antti Kiviniemi,1 Raija T. Laukkanen,3 Seppo Nissilä,3 Heikki V. Huikuri,2 and Mikko P. Tulppo1,2

1Merikoski Rehabilitation and Research Center, Oulu; 2Division of Cardiology, Department of Medicine, University of Oulu, Oulu; and 3Polar Electro, Kempele, Finland

Submitted 14 March 2003 ; accepted in final form 12 June 2003


   ABSTRACT
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 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
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 REFERENCES
 
Individual responses to aerobic training vary from almost none to a 40% increase in aerobic fitness in sedentary subjects. The reasons for these differences in the training response are not well known. We hypothesized that baseline cardiovascular autonomic function may influence the training response. The study population included sedentary male subjects (n = 39, 35 ± 9 yr). The training period was 8 wk, including 6 sessions/wk at an intensity of 70–80% of the maximum heart rate for 30–60 min/session. Cardiovascular autonomic function was assessed by measuring the power spectral indexes of heart rate variability from 24-h R-R interval recordings before the training period. Mean peak O2 uptake increased by 11 ± 5% during the training period (range 2–19%). The training response correlated with age (r = –0.39, P = 0.007) and with the values of the high-frequency (HF) spectral component of R-R intervals (HF power) analyzed over the 24-h recording (r = 0.46, P = 0.002) or separately during the daytime hours (r = 0.35, P = 0.028) and most strongly during the nighttime hours (r = 0.52, P = 0.001). After adjustment for age, HF power was still associated with the training response (e.g., P = 0.001 analyzed during nighttime hours). These data show that cardiovascular autonomic function is an important determinant of the response to aerobic training among sedentary men. High vagal activity at baseline is associated with the improvement in aerobic power caused by aerobic exercise training in healthy sedentary subjects.

cardiovascular autonomic function; vagal activity; aerobic training response

REGULAR PHYSICAL ACTIVITY and good physical fitness are widely accepted as factors that reduce all-cause mortality and improve a number of health outcomes (12). A recent study showed that low maximal aerobic capacity is closely related to an increase of untoward cardiac events (17). Therefore, physical training has been proposed to reduce these events by improving aerobic capacity. However, enormous heterogeneity in the responsiveness to physical training, assessed as the change in maximal O2 uptake (O2 max), has been observed, even in highly standardized training programs (5). Mean improvements to O2 max have been ~25% of the baseline values; these improvements range from no gain to a 40% increase in O2 max (3, 5). The physiological background for the wide range of responses to physical training remains unclear.

Assessment of heart rate (HR) variability from 24-h ambulatory ECG recordings is an effective and reproducible tool to study cardiovascular autonomic regulation in various clinical and physiological settings (2, 6, 10, 11, 13, 16, 30, 31). Time- and frequency-domain analyses of HR variability are the methods most commonly used to evaluate autonomic regulation.

In previous cross-sectional studies, the cardiovascular autonomic regulation was associated with aerobic fitness in a random population of healthy subjects (31) as well as in athletes (24). However, the association between training response and cardiovascular autonomic function is largely unknown. Therefore, the purpose of this study was to test the hypothesis that individual cardiac autonomic function may predict the response to aerobic training. We assessed 24-h HR variability among subjects who subsequently underwent standardized moderate- or high-volume aerobic exercise training.


   METHODS
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 METHODS
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Subjects. The subjects were recruited by advertising in a newspaper, which attracted 85 replies. All smokers, subjects with a high body mass index (BMI > 30), subjects who participated in regular physical training more than twice a week, and subjects with diabetes mellitus, asthma, or cardiovascular disorders were excluded. We invited 60 male subjects to our laboratory (Merikoski Rehabilitation and Research Center) for a more specific assessment of physical status and excluded 2 subjects because of various relative contraindications for a maximal exercise test. We tested 58 subjects and excluded 3 from the final analysis because of ectopic beats during the period of data acquisition. Finally, 55 men were included in the study. The subjects were randomized into a moderate-volume training group (n = 20), a high-volume training group (n = 20), and a control group (n = 15). One subject in the high-volume group and three subjects in the control group dropped out because of a lack of motivation or leg problems. The protocol was approved by the Ethics Committee of the Merikoski Rehabilitation and Research Center, and all subjects gave written informed consent.

Protocol. The subjects performed a graded maximal exercise test on a treadmill (Telineyhtymä, Kotka, Finland) at a work rate that started at 4.5 km/h and increased in 0.5 km/h increments every 2 min until exhaustion. The subjects were encouraged to perform at maximal effort. Ventilation and gas exchange (ergospirometer, model M909, Medikro, Kuopio, Finland) were monitored continuously during the protocol. The highest value of O2 uptake measured during the test (1-min collection) was taken as the peak O2 uptake (O2 peak). Nineteen subjects in the training group achieved a plateau in their O2 uptake in both tests. Twenty subjects did not reach a plateau in one or two tests. However, all the subjects fulfilled the criteria for O2 peak given in the literature: respiratory exchange ratio >1.1 or maximum HR (HRmax) within ±10 beats of the age-appropriate reference value (8). All physical exercise and alcohol were forbidden for 48 h before the day of exercise testing.

R-R intervals were recorded before the exercise testing over 24 h with an R-R recorder (Polar Electro) at an accuracy of 1 ms (23) and saved in a computer for further analysis of HR variability with HEARTS software (Heart Signal, Kempele, Finland). All R-R intervals were edited by visual inspection based on ECG portions to exclude all undesirable beats, which accounted for <2% in every subject. Measures of R-R interval dynamics were calculated from the entire 24-h recording and also separately for the hours representing the nighttime (midnight to 6 AM) and daytime (9 AM–6 PM) hours to detect possible diurnal differences (20).

The mean HR and the standard deviation of all R-R intervals were used as time-domain measures of HR variability. An autoregressive model was used to estimate the power spectrum densities of R-R interval variability, and the average 24-h values were calculated from the segments of 512 R-R intervals (9). Ultra-low-frequency (LF) power (<0.0033 Hz), very-LF power (0.0033–0.04 Hz), LF power (0.04–0.15 Hz), and high-frequency (HF) power (0.15–0.4 Hz) values were calculated from the entire 24-h segment. LF and HF power were also calculated from 1-h segments of the 24-h recording (using segments of 512 R-R intervals), and the mean values of these segments were used to detect day and night HR variability values (20). The spectral values are expressed as absolute values.

Training program. The training period was 8 wk long, including six 30-min sessions per week for the moderate-volume training group and six 60-min sessions per week for the high-volume training group at an intensity of 70–80% of HRmax. The individual HRmax was established on the basis of the HRmax achieved during the O2 peak test. The American College of Sports Medicine recommends 20–60 min of aerobic training for sedentary subjects (1). The purpose of our design was to induce a wide range of changes in aerobic fitness in sedentary subjects on the basis of American College of Sports Medicine recommendations. The training mode was walking and jogging. All the subjects wore a telemetric HR monitor (Polar Smart Edge, Polar Electro) during all the training sessions to reach and retain the correct training intensity.

Statistical methods. Values are means ± SD. The normal Gaussian distribution of the data was verified by the Kolmogorov-Smirnov goodness-of-fit test. The spectral values of HR variability were skewed. Therefore, the natural logarithms of the absolute values were taken to transform these data. The differences within the groups after training were analyzed by a two-factor analysis of variance with time and interventions followed by post hoc analysis (Student's paired t-test). Pearson's bivariate correlation analysis was performed between the baseline status of age, BMI, O2 peak, training response ({Delta}O2 peak), and different HR variability parameters.

{Delta}O2 peak was adjusted for the effects of covariates using a stepwise linear regression procedure for baseline age, together with the HR variability indexes. Each HR variability parameter that correlated with the training response was tested separately in a linear regression analysis procedure because of the high correlation between the different HR variability indexes (28). When the training group was divided into quartiles according to {Delta}O2 peak, analysis of variance was followed by post hoc analysis of Bonferroni's t-test comparing the differences between the groups. P < 0.05 was considered statistically significant.


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DISCUSSION
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The individual training responses are shown in Fig. 1. The average increase in O2 peak was 11 ± 5% (range 2–19%; Table 1). The training response did not differ between the moderate- and high-volume training groups. None of the measured variables changed within the control group during the study.



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  		Fig. 1. Heterogeneity of peak O2 uptake (O2peak) training responses after 8 wk of controlled aerobic training in healthy sedentary men.

 

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  		Table 1. Effects of training on O2 peak, maximal respiratory exchange ratio, and BMI

 

Contribution of HR variability to the training response. The training response correlated with age (r = –0.39, P = 0.007), but not with the baseline level of O2 peak or BMI (r = –0.06 and –0.12, respectively, not significant for both). Age accounted for 16% of the change as an independent predictor of the aerobic training response, and the corresponding values for O2 peak and BMI were 0.4 and 1.4%. A significant correlation was observed between the training response and the baseline HF power of R-R intervals analyzed over the 24-h recording (r = 0.46, P = 0.002) during the nighttime (r = 0.52, P = 0.001) and daytime (r = 0.35, P = 0.028) hours. Also, the LF power during the nighttime hours (r = 0.38, P = 0.018) and the very-low-frequency power over 24 h (r = 0.34, P = 0.017) were related to the training response. After adjustment for age, only HF power was associated with the training response (Fig. 2). HF power during the nighttime hours accounted for 27% (P = 0.001) of the change as an independent predictor of the aerobic training response. The correlations between the training response and the mean HR, standard deviation of all R-R intervals, or ultra-LF power were not significant under any conditions.



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  		Fig. 2. Correlation coefficients after adjustment for age between the interindividual training response ({Delta}O2peak) and the natural logarithm of high-frequency (HF) power during nighttime (midnight to 6 AM) (A), during daytime (9 AM–6 PM) (B), and over 24 h (C). A stepwise linear regression procedure was used to study adjustment for age, baseline O2peak, body mass index, and each heart rate variability parameter. {circ}, Moderate-volume training group; {bullet}, high-volume training group.

 

Baseline HR variability indexes in quartiles according to the training response. The study group was also divided into quartiles according to the training response (17 ± 1, 11 ± 1, 8 ± 1, and 5 ± 2% increase in O2 peak, P < 0.001 between groups). HF power at baseline analyzed over 24 h or during the nighttime hours was higher among the group with the best training response than among the group with lower responses (Table 2). The groups did not differ from each other in terms of baseline O2 peak, age, and BMI (Table 2).


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  		Table 2. Characteristics of subjects in the different individual aerobic training response ({Delta} O2 peak) quartiles and HR variability indexes at baseline over 24 h

 


   DISCUSSION
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 DISCUSSION
DISCLOSURES
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The main finding of this study was that 24-h HR dynamics at baseline, particularly the vagally mediated HF power spectral component, are associated with the improvement in aerobic power caused by aerobic exercise training in healthy sedentary subjects. There was a relation between the baseline HR variability indexes, such as the HF power spectral component, and the training response, suggesting that cardiovascular autonomic regulation is an important determinant of training response to physical exercise.

Individual responses to aerobic training. Large individual differences in the response to regular aerobic training have been observed after highly standardized exercise programs in healthy sedentary subjects (5, 14, 15). Consistent with the previous studies, we also found a large variation in the training response after a controlled aerobic training intervention in healthy sedentary men. The HERITAGE Family Study, based on 720 healthy sedentary subjects, summarized the contributions of age, gender, race, and baseline fitness level to the response to aerobic training. All these variables together accounted for only 11% of the variance in the response to 20 wk of standardized training. The subject's gender was the most powerful predictor of the training response, with a contribution of 5.4%, followed by age, with a contribution of 4% (5). In our male population, age accounted for 16% of the response as an independent predictor of the aerobic training response. Our training intervention was short (8 wk) compared with that of the HERITAGE Family Study (20 wk), which may emphasize the importance of age on the short-term training response. The age range of our subjects was large (23–52 yr) compared with the age ranges in training studies performed with older healthy sedentary individuals (60–71 yr) (14) and younger subjects (21–29 yr) (15). In agreement with the previous studies, the baseline fitness level was not significantly associated with the training response in the present study.

The American College of Sports Medicine recommends that the duration of a single aerobic training session should be 20–60 min for sedentary subjects (1). In the present study, however, both modes of training (30 and 60 min/session) resulted in similar changes of aerobic fitness in sedentary subjects. Our results show that the response to an aerobic training intervention in sedentary subjects is not dependent on the volume of training but, rather, must be determined by other factors.

Cardiovascular autonomic regulation as a determinant of training response. The total HR variability has been shown to decrease by 80–90% after complete vagal blockade. Therefore, vagal activity has been proposed to be the major determinant of HR variability in healthy humans (7, 29). Efferent cardiac vagal outflow has been generally proposed to contribute to the HF spectral power of HR variability (7, 28). In the present study, baseline HF power during the nighttime hours was the most powerful HR variability index associated with the future training response, accounting for 27% of the change as an independent predictor of the aerobic training response. This is an important finding, because the nighttime hours reflect a more standardized condition, and the results are less influenced by the subject's behavioral pattern. Together, these findings support the concept that cardiac vagal activity is an important determinant of the training response in sedentary men.

Possible mechanisms for individual cardiovascular adaptation. The mechanisms underlying the relation between the baseline vagal activity and the training response remain speculative. In accordance with the large interindividual variation in the training response to physical exercise, wide intersubject variation has also been observed in cardiovascular autonomic regulation in healthy subjects when measured by the HR variability indexes (20). Recent studies have shown that genetic factors may determine a large proportion (>20%) of the interindividual variation of R-R interval variability (25, 26), whereas demographic and other factors, including blood pressure, blood cholesterol, cardiac dimensions, BMI, and smoking, explain only a small proportion (~10%) of this variation in autonomic regulation (19). Similarly, it is well known that genetic background causes considerable variation in the baseline aerobic capacity and the changes in aerobic fitness after exercise training interventions (4, 21, 22). Therefore, there might be a common denominator that explains partly adaptation to aerobic training and HR variability. Genetic factors are the major candidates for this denominator.

A mechanistic link between the cardiac vagal function and the training response is also possible. In those subjects with good vagal function, the cardiovascular system may have a better capacity to adapt to various external stimuli, e.g., physical exercise. This adaptation capacity may improve overall cardiovascular performance after the regular physical training, thereby also improving the aerobic fitness. This hypothesis should be confirmed in future experimental studies.

Study limitations. In the present study, we investigated the differences in HR variability and training response only in healthy men. However, there are no significant differences in aerobic training responses between men and women (18, 27), and we decided to start with healthy men, because it may be important to understand the association between the training response and autonomic regulation in a homogeneous sample of subjects. An obvious limitation of the study is that the test subjects' age range was relatively large, which must be taken into consideration in interpretation of the results.

Conclusion. The present observations provide novel information on the contribution of the cardiovascular autonomic function to the training response. These observations may have some practical implications. For example, measurement of autonomic function may become important in designing individual training programs. However, the present findings are still preliminary and should be confirmed in future studies with different training programs and in various populations before generalization of the results. Finally, more experimental work is needed to understand the possible mechanistic link between the cardiovascular autonomic function and the training response.


   DISCLOSURES
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 ABSTRACT
 METHODS
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 DISCUSSION
 DISCLOSURES
REFERENCES
 
The authors appreciate the technical and financial support received from Polar Electro and the generous help from Heart Signal (Kempele, Finland). This research was funded by grants from the Ministry of Education (Helsinki, Finland) and the Medical Council of the Academy of Finland (Helsinki, Finland).


   FOOTNOTES
 

Address for reprint requests and other correspondence: M. P. Tulppo, Merikoski Rehabilitation and Research Center, Kasarmintie 13, 90100 Oulu, Finland (E-mail: mikko.tulppo{at}merikoski.fi).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


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  1. American College of Sports Medicine. Position statement on the recommended quality and quantity of exercise developing and maintaining cardiorespiratory and muscular fitness, and flexibility in healthy adults. Med Sci Sports Exerc 22: 265–274, 1998.
  2. Bigger JT, Fleiss JL Jr, Steinman RC, Rolnitzky LM, Kleiger RE, and Rottman JN. Correlations among time and frequency domain measures of heart period variability two weeks after acute myocardial infarction. Am J Cardiol 69: 891–898, 1992.[ISI][Medline]
  3. Bouchard C. Individual differences in the response to regular exercise. Int J Obes 19, Suppl: S5–S8, 1995.
  4. Bouchard C, An P, Rice T, Skinner JS, Wilmore JH, Gagnon J, Perusse L, Leon AS, and Rao DC. Familial aggregation of O2 max response to exercise training: results from the HERITAGE Family Study. J Appl Physiol 87: 1003–1008, 1999.[Abstract/Free Full Text]
  5. Bouchard C and Rankinen T. Individual differences in response to regular physical activity. Med Sci Sports Exerc 33 Suppl: 446–451, 2001.
  6. Hautala A, Tulppo MP, Mäkikallio TH, Laukkanen R, Nissilä S, and Huikuri HV. Changes in cardiac autonomic regulation after prolonged maximal exercise. Clin Physiol 21: 238–245, 2001.[ISI][Medline]
  7. Hayano JY, Sakakibara A, Yamada M, Mukai S, Fujinami T, Yokahama K, Watanabe Y, and Takata K. Accuracy of assessment of cardiac vagal tone by heart rate variability in normal subjects. Am J Cardiol 67: 199–204, 1991.[ISI][Medline]
  8. Howley ED, Bassett DR Jr, and Welch HG. Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc 27: 1292–1301, 1995.[ISI][Medline]
  9. Huikuri HV, Linnaluoto MK, Seppänen T, Airaksinen KE, Kessler KM, Takkunen JT, and Myerburg RJ. Circadian rhythm of heart rate variability in survivors of cardiac arrest. Am J Cardiol 70: 610–615, 1992.[ISI][Medline]
  10. Huikuri HV, Mäkikallio TH, Airaksinen KE, Seppänen T, Puukka P, Räihä IJ, and Sourander LB. Power-law relationship of heart rate variability as a predictor of mortality in the elderly. Circulation 97: 2031–2036, 1998.[Abstract/Free Full Text]
  11. Huikuri HV, Mäkikallio TH, Peng CK, Goldberger AL, Hintze U, and Moller M. Fractal correlation properties of R-R interval dynamics and mortality in patients with depressed left ventricular function after an acute myocardial infarction. Circulation 101: 47–53, 2000.[Abstract/Free Full Text]
  12. Kesäniemi A, Danforth E Jr, Jensen MD, Kopelman PG, Lefebre P, and Reeder BA. Dose-response issues concerning physical activity and health: an evidence-based symposium. Med Sci Sports Exerc 33, Suppl: 351–359, 2001.
  13. Kleiger RE, Miller JP, Bigger JT Jr, and Moss AJ. Decreased heart rate variability and its association with increased mortality after acute myocardial infarction. Am J Cardiol 59: 256–262, 1987.[ISI][Medline]
  14. Kohrt WM, Malley MT, Coggan AR, Spina RJ, Ogawa T, Ehsani A, Bourey RE, Martin WH III, and Holloszy JO. Effects of gender, age, and fitness level on response of O2 max to training in 60–71 yr olds. J Appl Physiol 71: 2004–2011, 1991.[Abstract/Free Full Text]
  15. Lortie G, Simoneau JA, Hamel P, Boulay MR, Landry F, and Bouchard C. Responses of maximal aerobic power and capacity to aerobic training. Int J Sports Med 5: 232–236, 1984.[ISI][Medline]
  16. Mäkikallio TH, Koistinen J, Jordaens L, Tulppo MP, Wood N, Golosarsky B, Peng CK, Goldberger AL, and Huikuri HV. Heart rate dynamics before spontaneous onset of ventricular fibrillation in patients with healed myocardial infarcts. Am J Cardiol 83: 880–884, 1999.[ISI][Medline]
  17. Myers J, Prakash M, Froelicher V, Do D, Partington S, and Atwood JE. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med 346: 793–801, 2002.[Abstract/Free Full Text]
  18. O'Toole ML. Gender differences in the cardiovascular response to exercise. Cardiovasc Clin 19: 17–33, 1989.[Medline]
  19. Pikkujämsä SM, Mäkikallio TH, Airaksinen KE, and Huikuri HV. Determinants and interindividual variation of R-R interval dynamics in healthy middle-aged subjects. Am J Physiol Heart Circ Physiol 280: H1400–H1406, 2001.[Abstract/Free Full Text]
  20. Pikkujämsä SM, Mäkikallio TH, Sourander LB, Räihä IJ, Puukka P, Skyttä J, Peng CK, Goldberger AL, and Huikuri HV. Cardiac interbeat interval dynamics from childhood to senescence: comparison of conventional and new measures based on fractals and chaos theory. Circulation 100: 393–399, 1999.[Abstract/Free Full Text]
  21. Rankinen T, Perusse L, Rauramaa R, Rivera MA, Wolfarth B, and Bouchard C. The human gene map for performance and health-related fitness phenotypes. Med Sci Sports Exerc 6: 855–867, 2001.
  22. Rankinen T, Perusse L, Rauramaa R, Rivera MA, Wolfarth B, and Bouchard C. The human gene map for performance and health-related fitness phenotypes: the 2001 update. Med Sci Sports Exerc 8: 1219–1233, 2002.
  23. Ruha A, Sallinen S, and Nissilä S. A real-time microprocessor QRS detector system with a 1-ms timing accuracy for the measurement of ambulatory HRV. IEEE Trans Biomed Eng 44: 159–167, 1997.[ISI][Medline]
  24. Shin K, Minamitani S, Onishi S, Yamazaki H, and Lee M. Autonomic differences between athletes and nonathletes: spectral analysis approach. Med Sci Sports Exerc 11: 1482–1490, 1997.
  25. Singh JP, Larson MG, O'Donnell CJ, Tsuji H, Evans JC, and Levy D. Heritability of heart rate variability. The Framingham Heart Study. Circulation 99: 2251–2254, 1999.[Abstract/Free Full Text]
  26. Singh JP, Larson MG, O'Donnell CJ, Tsuji H, Corey D, and Levy D. Genome scan linkage results for heart rate variability (the Framingham Heart Study). Am J Cardiol 90: 1290–1293, 2002.[ISI][Medline]
  27. Skinner JS, Jaskolski A, Jaskolska A, Krasnoff J, Gagnon J, Leon A, Rao RD, Willmore JH, and Bouchard C. HERITAGE Family Study. Age, sex, race, initial fitness, and response to training: the HERITAGE Family Study. J Appl Physiol 90: 1770–1776, 2001.[Abstract/Free Full Text]
  28. Task Force of the European Society of Cardiology, and the North American Society of Pacing and Electrophysiology. Heart rate variability, standards of measurement, physiological interpretation and clinical use. Circulation 93: 1043–1065, 1996.[Free Full Text]
  29. Taylor JA, Carr DL, Myers CW, and Eckberg DL. Mechanics underlying very-low-frequency R-R interval oscillations in humans. Circulation 98: 547–555, 1998.[Abstract/Free Full Text]
  30. Tulppo MP, Hughson R, Mäkikallio T, Airaksinen J, Seppänen T, and Huikuri HV. Effects of exercise and passive head-up tilt on fractal and complexity properties of heart rate dynamics. Am J Physiol Heart Circ Physiol 280: H1081–H1087, 2001.[Abstract/Free Full Text]
  31. Tulppo MP, Mäkikallio TH, Seppänen T, Laukkanen RT, and Huikuri HV. Vagal modulation of heart rate during exercise: effects of age and physical fitness. Am J Physiol Heart Circ Physiol 274: H424–H429, 1998.[Abstract/Free Full Text]



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