Abstract
Purpose
High cardiac vagal control in endurance athletes has been generally associated with adequate recovery from training and readiness to cope high-intensity training. A method that improves cardiac vagal control in endurance athletes could therefore be advantageous. Accordingly, we sought to test whether ischemic preconditioning (IPC) could enhance cardiac vagal control in endurance runners.
Methods
Fifteen subjects underwent IPC, sham ultrasound (SHAM) or control (CT), in random order. Subjects were informed both IPC and SHAM would be beneficial vs. CT (i.e., similar placebo induction), and IPC would be harmless despite ischemia sensations (i.e., nocebo avoidance). Resting cardiac vagal control was assessed via respiratory sinus arrhythmia (RSA) and heart rate variability (HRV) indexes. Post-exercise cardiac vagal control was assessed via heart rate recovery [HR time constant decay (T30) and absolute HR decay (HRR30s)] during 30-s breaks of a discontinuous incremental test. Capillary blood samples were collected for lactate threshold identification.
Results
RSA and HRV were similar among interventions at pre- and post-intervention assessments. Lactate threshold occurred at 85 ± 4% of maximal effort. T30 was similar among interventions, but IPC increased HRR30s at 70% and 75% of maximal effort vs. SHAM and CT (70%: IPC = 31 ± 2 vs. SHAM = 26 ± 3 vs. CT = 26 ± 2 bpm, mean ± SEM, P < 0.01; 75%: IPC = 29 ± 2 vs. SHAM = 25 ± 2 vs. CT = 24 ± 2 bpm, P < 0.01).
Conclusion
IPC did not change resting cardiac vagal control, but boosted fast post-exercise cardiac vagal reactivation at exercise intensities below lactate threshold in endurance runners.
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Abbreviations
- ANOVA:
-
Analysis of variance
- CT:
-
Resting control
- CV:
-
Coefficient of variation
- E/I max :
-
Ratio between the longest R–R interval among all expirations and the shortest R–R interval among all inspirations
- E/I mean :
-
Ratio between the mean of the longest R–R interval of each expiration and the mean of the shortest R–R interval of each inspiration
- HF:
-
High frequency
- HR:
-
Heart rate
- HRex:
-
Heart rate at the end of a given stage of the discontinuous incremental
- HRR:
-
Heart rate recovery
- HRR30s:
-
Heart rate recovery at 30 s post-exercise
- HRR60s:
-
Heart rate recovery at 60 s post-exercise
- HRV:
-
Heart rate variability
- ICC:
-
Intra-class correlation coefficient
- IPC:
-
Ischemic preconditioning
- LF:
-
Low frequency
- LF/HF:
-
Ratio between low- and high-frequency powers of heart rate variability
- Ln:
-
Natural logarithm of the RMSSD was divided by the mean R–R interval
- RMSSD:
-
Square root of the mean squared differences between consecutive R–R intervals
- RRi:
-
R–R intervals
- RSA:
-
Respiratory sinus arrhythmia
- SEM:
-
Standard error of the mean
- SHAM:
-
Sham ultrasound
- SWC:
-
Smallest worthwhile change
- TP:
-
Total power
- T30:
-
Time constant of heart rate decay
- VLF:
-
Very low frequency
- \(\dot {V}{{\text{O}}_{{\text{2max}}}}\) :
-
Maximal oxygen consumption
References
Akselrod S, Gordon D, Ubel FA, Shannon DC, Berger AC, Cohen RJ (1981) Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science 213:220–222. https://doi.org/10.1126/science.6166045
Arai Y, Saul JP, Albrecht P, Hartley LH, Lilly LS, Cohen RJ, Colucci WS (1989) Modulation of cardiac autonomic activity during and immediately after exercise. Am J Physiol 256:H132–H141. https://doi.org/10.1152/ajpheart.1989.256.1.H132
Aubry A, Hausswirth C, Louis J, Coutts AJ, Buchheit M, Le Meur Y (2015) The development of functional overreaching is associated with a faster heart rate recovery in endurance athletes. PLoS One 10:e0139754. https://doi.org/10.1371/journal.pone.0139754
Basalay M, Barsukevich V, Mastitskaya S, Mrochek A, Pernow J, Sjoquist PO, Ackland GL, Gourine AV, Gourine A (2012) Remote ischaemic pre- and delayed postconditioning—similar degree of cardioprotection but distinct mechanisms. Exp Physiol 97:908–917. https://doi.org/10.1113/expphysiol.2012.064923
Beedie CJ, Stuart EM, Coleman DA, Foad AJ (2006) Placebo effects of caffeine on cycling performance. Med Sci Sports Exerc 38:2159–2164. https://doi.org/10.1249/01.mss.0000233805.56315.a9
Bellenger CR, Fuller JT, Thomson RL, Davison K, Robertson EY, Buckley JD (2016) Monitoring athletic training status through autonomic heart rate regulation: A systematic review and meta-analysis. Sports Med 46:1461–1486. https://doi.org/10.1007/s40279-016-0484-2
Benedetti F (2013) Placebo and the new physiology of the doctor-patient relationship. Physiol Rev 93:1207–1246. https://doi.org/10.1152/physrev.00043.2012
Boullosa DA, Barros ES, del Rosso S, Nakamura FY, Leicht AS (2014) Reliability of heart rate measures during walking before and after running maximal efforts. Int J Sports Med 35:999–1005. https://doi.org/10.1055/s-0034-1372637
Buchheit M (2014) Monitoring training status with HR measures: do all roads lead to Rome? Front Physiol. https://doi.org/10.3389/fphys.2014.00073
Buchheit M, Laursen PB, Ahmaidi S (2007) Parasympathetic reactivation after repeated sprint exercise. Am J Physiol Heart Circ Physiol 293:H133–H141. https://doi.org/10.1152/ajpheart.00062.2007
Carter R 3rd, Watenpaugh DE, Wasmund WL, Wasmund SL, Smith ML (1999) Muscle pump and central command during recovery from exercise in humans. J Appl Physiol 87:1463–1469. https://doi.org/10.1152/jappl.1999.87.4.1463
Chen L, Zhou Q, Jin H, Zhu K, Zhi H, Chen Z, Ma G (2018) Effects of remote ischaemic conditioning on heart rate variability and cardiac function in patients with mild ischaemic heart failure. Heart Lung Circ 27:477–483. https://doi.org/10.1016/j.hlc.2017.03.164
Clark VR, Hopkins WG, Hawley JA, Burke LM (2000) Placebo effect of carbohydrate feedings during a 40-km cycling time trial. Med Sci Sports Exerc 32:1642–1647
Daanen HA, Lamberts RP, Kallen VL, Jin A, Van Meeteren NL (2012) A systematic review on heart-rate recovery to monitor changes in training status in athletes. Int J Sports Physiol Perform 7:251–260. https://doi.org/10.1123/ijspp.7.3.251
De Meersman RE (1992) Respiratory sinus arrhythmia alteration following training in endurance athletes. Eur J Appl Physiol Occup Physiol 64:434–436. https://doi.org/10.1007/BF00625063
de Castro CL, de Nobrega AC, de Araujo CG (1992) [Autonomic cardiovascular tests. A critical review. I]. Arq Bras Cardiol 59:75–85
Draper DO, Castel JC, Castel D (1995) Rate of temperature increase in human muscle during 1 MHz and 3 MHz continuous ultrasound. J Orthop Sports Phys Ther 22:142–150. https://doi.org/10.2519/jospt.1995.22.4.142
Dupuy O, Mekary S, Berryman N, Bherer L, Audiffren M, Bosquet L (2012) Reliability of heart rate measures used to assess post-exercise parasympathetic reactivation. Clin Physiol Funct Imaging 32:296–304. https://doi.org/10.1111/j.1475-097X.2012.01125.x
Enko K, Nakamura K, Yunoki K, Miyoshi T, Akagi S, Yoshida M, Toh N, Sangawa M, Nishii N, Nagase S, Kohno K, Morita H, Kusano KF, Ito H (2011) Intermittent arm ischemia induces vasodilatation of the contralateral upper limb. J Physiol Sci 61:507–513. https://doi.org/10.1007/s12576-011-0172-9
Ferreira TN, Sabino-Carvalho JL, Lopes TR, Ribeiro IC, Succi JE, da Silva AC, Silva BM (2016) Ischemic preconditioning and repeated sprint swimming: a placebo and nocebo study. Med Sci Sports Exerc 48:1967–1975. https://doi.org/10.1249/mss.0000000000000977
Gourine A, Gourine AV (2014) Neural mechanisms of cardioprotection. Physiology 29:133–140. https://doi.org/10.1152/physiol.00037.2013
Grossman P, Karemaker J, Wieling W (1991) Prediction of tonic parasympathetic cardiac control using respiratory sinus arrhythmia: the need for respiratory control. Psychophysiology 28:201–216. https://doi.org/10.1111/j.1469-8986.1991.tb00412.x
Imai K, Sato H, Hori M, Kusuoka H, Ozaki H, Yokoyama H, Takeda H, Inoue M, Kamada T (1994) Vagally mediated heart rate recovery after exercise is accelerated in athletes but blunted in patients with chronic heart failure. J Am Coll Cardiol 24:1529–1535. https://doi.org/10.1016/0735-1097(94)90150-3
Incognito AV, Burr JF, Millar PJ (2016) The effects of ischemic preconditioning on human exercise performance. Sports Med 46:531–544. https://doi.org/10.1007/s40279-015-0433-5
Kannankeril PJ, Le FK, Kadish AH, Goldberger JJ (2004) Parasympathetic effects on heart rate recovery after exercise. J Investig Med 52:394–401. https://doi.org/10.1136/jim-52-06-34
Kentta G, Hassmen P (1998) Overtraining and recovery. A conceptual model. Sports Med 26:1–16. https://doi.org/10.2165/00007256-199826010-00001
Kiviniemi AM, Hautala AJ, Kinnunen H, Nissila J, Virtanen P, Karjalainen J, Tulppo MP (2010) Daily exercise prescription on the basis of HR variability among men and women. Med Sci Sports Exerc 42:1355–1363. https://doi.org/10.1249/MSS.0b013e3181cd5f39
Le Meur Y, Buchheit M, Aubry A, Coutts AJ, Hausswirth C (2017) Assessing overreaching with heart-rate recovery: what is the minimal exercise intensity required? Int J Sports Physiol Perform 12:569–573. https://doi.org/10.1123/ijspp.2015-0675
Lee CM, Mendoza A (2012) Dissociation of heart rate variability and heart rate recovery in well-trained athletes. Eur J Appl Physiol 112:2757–2766. https://doi.org/10.1007/s00421-011-2258-8
Lopes TR, Sabino-Carvalho JL, Ferreira TN, Succi JE, Silva AC, Silva BM (2018) Effect of ischemic preconditioning on the recovery of cardiac autonomic control from repeated sprint exercise. Front Physiol 9:1465. https://doi.org/10.3389/fphys.2018.01465
Loukogeorgakis SP, Panagiotidou AT, Broadhead MW, Donald A, Deanfield JE, MacAllister RJ (2005) Remote ischemic preconditioning provides early and late protection against endothelial ischemia-reperfusion injury in humans: role of the autonomic nervous system. J Am Coll Cardiol 46:450–456. https://doi.org/10.1016/j.jacc.2005.04.044
Machhada A, Trapp S, Marina N, Stephens RCM, Whittle J, Lythgoe MF, Kasparov S, Ackland GL, Gourine AV (2017) Vagal determinants of exercise capacity. Nat Commun 8:15097. https://doi.org/10.1038/ncomms15097
Mastitskaya S, Marina N, Gourine A, Gilbey MP, Spyer KM, Teschemacher AG, Kasparov S, Trapp S, Ackland GL, Gourine AV (2012) Cardioprotection evoked by remote ischaemic preconditioning is critically dependent on the activity of vagal pre-ganglionic neurones. Cardiovasc Res 95:487–494. https://doi.org/10.1093/cvr/cvs212
Medigue C, Girard A, Laude D, Monti A, Wargon M, Elghozi JL (2001) Relationship between pulse interval and respiratory sinus arrhythmia: a time- and frequency-domain analysis of the effects of atropine. Pflugers Arch 441:650–655. https://doi.org/10.1007/s004240000486
Newell J, Higgins D, Madden N, Cruickshank J, Einbeck J, McMillan K, McDonald R (2007) Software for calculating blood lactate endurance markers. J Sports Sci 25:1403–1409. https://doi.org/10.1080/02640410601128922
Paiva VC, Santana KR, Silva BM, Ramos PS, Lovisi JC, Araujo CG, Ricardo DR (2011) Comparison of assessment methods of cardiac vagal modulation. Arq Bras Cardiol 97:493–501. https://doi.org/10.1590/S0066-782X2011005000109
Pecanha T, Forjaz CLM, Low DA (2017) Passive heating attenuates post-exercise cardiac autonomic recovery in healthy young males. Front Neurosci 11:727. https://doi.org/10.3389/fnins.2017.00727
Rabbani A, Kargarfard M, Twist C (2018) Reliability and validity of a submaximal warm-up test for monitoring training status in professional soccer players. J Strength Cond Res 32:326–333. https://doi.org/10.1519/jsc.0000000000002335
Sabino-Carvalho JL, Barbosa TC, Silva BM (2015) What is the effect of ischemic preconditioning on the kinetics of pulmonary oxygen uptake and muscle deoxygenation during exercise? Physiol Rep. https://doi.org/10.14814/phy2.12540
Sabino-Carvalho JL, Lopes TR, Obeid-Freitas T, Ferreira TN, Succi JE, Silva AC, Silva BM (2017) Effect of ischemic preconditioning on endurance performance does not surpass placebo. Med Sci Sports Exerc 49:124–132. https://doi.org/10.1249/mss.0000000000001088
Silva BM, Neves FJ, Negrao MV, Alves CR, Dias RG, Alves GB, Pereira AC, Rondon MU, Krieger JE, Negrao CE, Nobrega AC (2011) Endothelial nitric oxide synthase polymorphisms and adaptation of parasympathetic modulation to exercise training. Med Sci Sports Exerc 43:1611–1618. https://doi.org/10.1249/MSS.0b013e3182152197
Task Force (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation 93:1043–1065. https://doi.org/10.1161/01.CIR.93.5.1043
Turcato S, Turnbull L, Wang GY, Honbo N, Simpson PC, Karliner JS, Baker AJ (2006) Ischemic preconditioning depends on age and gender. Basic Res Cardiol 101:235–243. https://doi.org/10.1007/s00395-006-0585-4
Vesterinen V, Nummela A, Ayramo S, Laine T, Hynynen E, Mikkola J, Hakkinen K (2016a) Monitoring training adaptation with a submaximal running test under field conditions. Int J Sports Physiol Perform 11:393–399. https://doi.org/10.1123/ijspp.2015-0366
Vesterinen V, Nummela A, Heikura I, Laine T, Hynynen E, Botella J, Hakkinen K (2016b) Individual endurance training prescription with heart rate variability. Med Sci Sports Exerc 48:1347–1354. https://doi.org/10.1249/mss.0000000000000910
Yasuma F, Hayano J (2004) Respiratory sinus arrhythmia: why does the heartbeat synchronize with respiratory rhythm? Chest 125:683–690. https://doi.org/10.1378/chest.125.2.683
Zagidullin N, Scherbakova E, Safina Y, Zulkarneev R, Zagidullin S (2016) The impact of remote ischemic preconditioning on arterial stiffness and heart rate variability in patients with angina pectoris. J Clin Med 5. https://doi.org/10.3390/jcm5070060
Acknowledgements
The time and effort expended by all the volunteer subjects is greatly appreciated.
Funding
J.L.S. and M.P. received scholarship from the Coordination for Improvement of Higher Education Personnel (CAPES). J.L.S., M.P. and T.O. received scholarship from the São Paulo Research Foundation (FAPESP; grants: 2014/15877-8, 2015/22198-2 and 2015/03572-0, respectively). B.M.S received funding from FAPESP (Grant: 2014/25683-6) and CNPq (Grant: 461516/2014-4) to conduct the study.
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JLS, TRL and BMS conceived and designed research. JLS, TO, TRL and THNF conducted experiments. JLS, TO, MP and TRL analyzed data. All authors interpreted the results of experiments. JLS and BMS prepared the figures and tables. JLS, BMS drafted the manuscript. All authors edited, revised and approved the manuscript.
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Communicated by Massimo Pagani.
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Sabino-Carvalho, J.L., Obeid-Freitas, T., Paula-Ribeiro, M. et al. Ischemic preconditioning boosts post-exercise but not resting cardiac vagal control in endurance runners. Eur J Appl Physiol 119, 621–632 (2019). https://doi.org/10.1007/s00421-018-4052-3
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DOI: https://doi.org/10.1007/s00421-018-4052-3