Ischemic preconditioning reduces hemodynamic response during metaboreflex activation

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 310, Issue 9, 2016, Pages R777-R787

  Mulliri, Gabriele ^a   Sainas, Gianmarco ^a   Magnani, Sara ^a   Palazzolo, Girolamo ^a   Milia, Nicola ^a   Orrù, Andrea ^a   Roberto, Silvana ^a   Marongiu, Elisabetta ^a   Milia, Raffaele ^a   Crisafulli, Antonio ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Blood pressure; Cardiac preload; Fatigue; Myocardial contractility; Stroke volume

Indexed keywords

NITRIC OXIDE;

ADULT; ARTICLE; BLOOD PRESSURE; CONTROL EXERCISE RECOVERY SESSION TEST; CONTROLLED STUDY; DOPPLER ECHOCARDIOGRAPHY; EXERCISE RECOVERY; EXERCISE TEST; FOREARM BLOOD FLOW; HAND GRIP; HEART AFTERLOAD; HEART HEMODYNAMICS; HEART MUSCLE CONTRACTILITY; HEART MUSCLE REPERFUSION; HEART PRELOAD; HEART RATE; HEART STROKE VOLUME; HEMODYNAMIC PARAMETERS; HUMAN; HUMAN EXPERIMENT; IMPEDANCE CARDIOGRAPHY; ISCHEMIC PRECONDITIONING; MALE; MEAN ARTERIAL PRESSURE; METABOREFLEX; MUSCLE METABOLISM; MUSCLE REFLEX; NORMAL HUMAN; POSTEXERCISE MUSCLE ISCHEMIA TEST; PRIORITY JOURNAL; SYMPATHETIC TONE; VENOUS RETURN; EXERCISE; FATIGUE; HEART CONTRACTION; HEMODYNAMICS; MIDDLE AGED; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; SKELETAL MUSCLE;

ADULT; EXERCISE; FATIGUE; HEMODYNAMICS; HUMANS; ISCHEMIC PRECONDITIONING; MALE; MIDDLE AGED; MUSCLE, SKELETAL; MYOCARDIAL CONTRACTION; PHYSICAL EXERTION;

EID: 84984600013     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00429.2015     Document Type: Article

References (68)

1. Addison PD, Neligan PC, Ashrafpour H, Khan A, Zhong A, Moses M, Forrest CR, Pang CY. Noninvasive remote ischemic preconditioning for global protection of skeletal muscle against infarction. Am J Physiol Heart Circ Physiol 285: H1435-H1443, 2003.
2. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Group III and IV muscle afferents contribute to ventilatory and cardiovascular response rhythmic exercise in humans. J Appl Physiol 109: 966-976, 2010.
3. Amann M, Proctor LT, Sebranek JJ, Eldridge MW, Pegelow DF, Dempsey JA. Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise. J Appl Physiol 105: 1714-1724, 2008.
4. Amann M, Runnels S, Morgan DE, Trinity JD, Fjeldstad AS, Walter Wray D, Reese VR, Richardson RS. On the contribution of group III and IV muscle afferents to the circulatory response to rhythmic exercise in humans. J Physiol 589: 3855-3866, 2011.
5. Andreani CM, Hill JM, Kaufman MP. Responses of group III and IV afferents to dynamic exercise. J Appl Physiol 82: 1811-1817, 1997.
6. Asimakis GK, Innerd-McBridge K, Medellin G, Conti VR. Ischemic preconditioning attenuates acidosis and postischemic dysfunction in isolated rat heart. Am J Physiol Heart Circ Physiol 263: H887-H894, 1992.
7. Bailey TG, Birk GK, Cable NT, Atkinson G, Green DJ, Jones H, Thijssen DHJ. Remote ischemic preconditioning prevents reduction in brachial artery flow-mediated dilation after strenuous exercise. Am J Physiol Heart Circ Physiol 303: H533-H538, 2012.
8. Bailey TG, Jones H, Gregson W, Atkinson G, Cable NT, Thijssen DHJ. Effect of ischemic preconditioning on lactate accumulation and running performance. Med Sci Sport Exerc 44: 2084-2089, 2012.
9. Barbosa TC, Machado AC, Braz ID, Fernandes IA, Vianna LC, Nobrega AC, Silva BM. Remote ischemic preconditioning delays fatigue development during handgrip exercise. Scand J Med Sci Sports 25: 256-364, 2015.
10. Bastos BG, Williamson JW, Harrelson T, Nôbrega ACL. Left ventricular volumes and hemodynamic responses to postexercise ischemia in healthy humans. Med Sci Sports Exerc 32: 1114-1118, 2000.
11. Bernstein DP. A new stroke volume equation for thoracic electrical bioimpedance: theory and rationale. Crit Care Med 14: 904-909, 1986.
12. Christie J, Sheldahl LM, Tristani FE, Sagar KB, Ptacin MJ, Wann S. Determination of stroke volume and cardiac output during exercise: comparison of two-dimensional and Doppler echocardiography, Fick oxymetry, and thermodiluition. Circulation 76: 539-547, 1987.
13. Clevidence MW, Mowery RE, Kushnick MR. The effects of ischemic preconditioning on aerobic and anaerobic variables associated with submaximal cycling performance. Eur J Appl Physiol 112: 3649-3654, 2012.
14. Cohen GI, Pietrolungo JF, Thomas JD, Klein AL. A practical guide to assessment of ventricular diastolic function using Doppler echocardiography. J Am Coll Cardiol 27: 1753-1760, 1996.
15. Cohen MV, Baines CP, Downey JM. Ischemic preconditioning: from adenosine receptor to KATP channel. Ann Rev Physiol 62: 79-109, 2000.
16. Crisafulli A, Marongiu E, Ogho S. Cardiovascular reflexes activity, and their interaction during exercise. Biomed Res Int 2015, doi:10.1155/2015/394183.
17. Crisafulli A, Melis F, Orrù V, Lener R, Lai C, Concu A. Impedance cardiography for non invasive assessment of systolic time intervals during exercise. Sports Med Train Rehab 10: 13-27, 2001.
18. Crisafulli A, Melis F, Tocco F, Santoboni UM, Lai C, Angioy G, Lorrai L, Pittau G, Concu A, Pagliaro P. Exercise-induced and nitroglycerin-induced myocardial preconditioning improves hemodynamics in patients with angina. Am J Physiol Heart Circ Physiol 287: H235-H242, 2004.
19. Crisafulli A, Milia R, Lobina A, Caddeo M, Tocco F, Concu A, Melis F. Hemodynamic effect of metaboreflex activation in men after running above and below the velocity of the anaerobic threshold. Exp Physiol 93: 447-457, 2008.
20. Crisafulli A, Milia R, Vitelli S, Caddeo M, Tocco F, Melis F, Concu A. Hemodynamic responses to metaboreflex activation: insights from spinal cord-injured humans. Eur J Appl Physiol 106: 525-533, 2009.
21. Crisafulli A, Piras F, Filippi M, Piredda C, Chiappori P, Melis F, Milia R, Tocco F, Concu A. Role of heart rate and stroke volume during muscle metaboreflex-induced cardiac output increase: differences between activation during and after exercise. J Physiol Sci 61: 385-394, 2011.
22. Crisafulli A, Salis E, Tocco F, Melis F, Milia R, Pittau G, Caria MA, Solinas R, Meloni L, Pagliaro P, Concu A. Impaired central hemodynamic response and exaggerated vasoconstriction during muscle metaboreflex activation in heart failure patients. Am J Physiol Heart Circ Physiol 292: H2988-H2996, 2007.
23. Crisafulli A, Scott AC, Wensel R, Davos CH, Francis DP, Pagliaro P, Coats AJS, Concu A, Piepoli MF. Muscle metaboreflex-induced increases in stroke volume. Med Sci Sports Exerc 35: 221-228, 2003.
24. Crisafulli A, Tangianu F, Tocco F, Concu A, Mameli O, Mulliri G, Caria MA. Ischemic preconditioning of the muscle improves maximal exercise performance but not maximal oxygen uptake in humans. J Appl Physiol 111: 530-536, 2011.
25. Crisafulli A, Tocco F, Milia R, Angius L, Pinna M, Olla S, Roberto S, Marongiu E, Porcu M, Concu A. Progressive improvement in hemodynamic response to muscle metaboreflex in heart transplant recipients. J Appl Physiol 114: 421-427, 2013.
26. Dawn B, Bolli R. Role of nitric oxide in myocardial preconditioning. Ann NY Acc Sci 962: 18-41, 2002.
27. de Groot PCE, Thijssen DHJ, Sanchez M, Ellenkamp R, Hopman MTE. Ischemic preconditioning improves maximal performance in humans. Eur J Appl Physiol 108: 141-146, 2010.
28. Deutsch E, Berger M, Kussmaul WG, Hirshfeld JW, Herrman HC, Laskey WK. Adaptation to ischemia during percutaneous transluminal coronary angioplasty: clinical, hemodynamic, and metabolic features. Circulation 82: 2044-2051, 1990.
29. Ferrari M, Muthalib M, Quaresima V. The use of near-infrared spectroscopy in understanding skeletal muscle physiology: recent developments. Philos Trans A Math Phys Eng Sci 369: 4577-45790, 2011.
30. Fisher JP, Adlan AM, Shantsila A, Secher F, Sørensen H, Secher NH. Muscle metaboreflex and autonomic regulation of heart rate in humans. J Physiol 591: 3777-3788, 2003.
31. Fisher JP, Seifert T, Hartwich D, Young CN, Secher NH, Fadel PJ. Autonomic control of heart rate by metabolically sensitive skeletal muscle afferents in humans. J Physiol 588: 1117-1127, 2010.
32. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81: 1725-1789, 2001.
33. Gardin JM, Dabestani A, Takenaka K, Rohan MK, Knoll M, Russell D, Henry WL. Effect of imaging view and sample volume location on evaluation of mitral flow velocity by pulsed Doppler echocardiogaphy. Am J Cardiol 57: 1335-1339, 1986.
34. Gibson N, White J, Neish M, Murray A,. Effect of ischemic preconditioning on land-based sprinting in team-sport athletes. Int J Sprts Physiol Perform 8: 671-676, 2013.
35. Gledhill N, Cox D, Jamnik R. Endurance athletes’ stroke volume does not plateau: major advantage is diastolic function. Med Sci Sports Exerc 26: 1116-1121, 1994.
36. Hittinger EA, Maher JL, Nash MS, Perry AC, Signorile JF, Kressler J, Jacobs KA. Ischemic preconditioning does not improve peak exercise capacity at sea level or simulated high altitude in trained male cyclists. Appl Physiol Nutr Metab 40: 65-71, 2015.
37. Horiuchi M, Endo J, Thijssen DH. Impact of ischemic preconditioning on functional sympatholysis during handgrip exercise in humans. Physiol Rep 22: 3. pii: e12304, 2015.
38. Koole MAC, Aerts A, Praet J, Franken P, Dendale P, Block P. Venous pooling during nitrate-stimulated tilt testing in patients with vasovagal syncope. Europace 2: 343-345, 2000.
39. Ichinose MJ, Sala-Mercado JA, Coutsos M, Li ZH, Ichinose TK, Dawe E, O’Leary DS. Modulation of cardiac output alters the mechanisms of the muscle metaboreflex pressor response. Am J Physiol Heart Circ Physiol 298: H245-H250, 2010.
40. Iellamo F, Pizzinelli P, Massaro M, Raimondi G, Peruzzi G, Legramante JM. Muscle metaboreflex contribution to sinus node regulation during static exercise. Circulation 100: 27-32, 1999.
41. Jean-St-Michel E, Manlhiot C, Li J, Tropak M, Michelsen MM, Schmidt MR, McCrindle BW, Wells GD, Redington AN. Remote preconditioning improves maximal performance in highly-trained athletes. Med Sci Sports Exerc 43: 1280-1286, 2011.
42. Jones B, Dat M, Cooper CE. Underwater near-infrared spectroscopy measurements of muscle oxygenation: laboratory validation and preliminary observations in swimmers and triathletes. J Biomed Opt 2014; 19: 127002. doi:10.1117/1.JBO.19.12.127002.
43. Kaufman MP, Rybicki KJ. Discharge properties of group III and IV muscle afferents: their responses to mechanical and metabolic stimuli. Circ Res, Suppl 61: 160-165, 1987.
44. Kjeld T, Rasmussen MR, Jattu T, Nielsen HB, Secher NH. Ischemic preconditioning of one forearm enhances static and dynamic apnea. Med Sci Sports Exerc 46: 151-155, 2014.
45. Lalonde F, Curnier DY. Can anaerobic performance be improved by remote ischemic preconditioning? J Strength Cond Res 29: 80-85, 2015.
46. Leesar MA, Stoddard MF, Xuan YT, Tang XL, Bolli R. Nonelectrocardiographic evidence that both ischemic preconditioning and adenosine preconditioning exist in humans. J Am Coll Cardiol 42: 437-445, 2003.
47. Marongiu E, Crisafulli A. cardioprotection acquired through exercise: the role of ischemic preconditioning. Curr Cardiol Rev 10: 336-348, 2014.
48. Marongiu E, Piepoli MF, Milia R, Angius L, Pinna M, Bassareo P, Roberto S, Tocco F, Concu A, Crisafulli A. Effects of acute vasodilation on the hemodynamic response to muscle metaboreflex. Am J Physiol Heart Circ Physiol 305: H1387-H1396, 2013.
49. McNully CL, Moody WE, Wagenmakers AJ, Fisher JP. Effect of muscle metaboreflex activation on central hemodynamics and cardiac function in humans. App Physiol Nutr Metab 39: 861-870, 2014.
50. Milia R, Roberto S, Mulliri G, Loi A, Marcelli M, Sainas G, Milia N, Marongiu E, Crisafulli A. Effect of aging on hemodynamic response to metaboreflex activation. Eur J Appl Physiol 115: 1693-1703, 2015.
51. Moran D, Epstein Y, Keren G, Laor A, Sherez J, Shapir Y. Calculation of mean arterial pressure during exercise as a function of heart rate. Appl Human Sci 14: 293-295, 1995.
52. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124-1136, 1986.
53. Nishiyasu T, Ueno H, Nishiyasu M, Tan N, Morimoto K, Morimoto A, Deguchi T, Murakami N. Relationship between mean arterial pressure and muscle pH during forearm ischemia after sustained handgrip. Acta Physiol Scand 151: 143-148, 1994.
54. Nóbrega ACL, O’Leary DS, Silva BM, Marongiu E, Piepoli MF, Crisafulli A. Neural regulation of cardiovascular response to exercise: role of central command and peripheral afferents. Biomed Res Int 2014; article ID 478965, http://dx.doi.org/10.1155/2014/478965.
55. O’Leary DS, Augustyniak RA. Muscle metaboreflex increases ventricular performance in conscious dogs. Am J Physiol Heart Circ Physiol 275: H220-H224, 1998.
56. Paixao RC, da Mota GR, Marocolo M. Acute effect of ischemic preconditioning is detrimental to anaerobic performance in cyclists. Int J Sports Med 35: 912-915, 2014.
57. Pang CY, Yang RZ, Zhong A, Xu N, Boyd B, Forrest CR. Acute ischemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovasc Res 29: 782-788, 1995.
58. Parratt J, Vegh A. Pronounced antiarrhythmic effects of ischemic preconditioning. Cardioscience 5: 9-18, 1994.
59. Patterson SD, Bezodis NE, Glaister M, Pattison JR. The effect of ischemic preconditioning on repeated sprint cycling performance. Med Sci Sports Exerc 47: 1652-1658, 2015.
60. Peart JN, Headrick JP. Clinical cardioprotection and the value of conditioning responses. Am J Physiol Heart Circ Physiol 296: H1705-H1720, 2009.
61. Roberto S, Marongiu E, Pinna M, Angius L, Olla S, Bassareo P, Tocco F, Concu A, Milia R, Crisafulli A. Altered hemodynamics during muscle metaboreflex in young, type 1 diabetes patients. J Appl Physiol 113: 1323-1331, 2012.
62. Sala-Mercado JA, Hammond RL, Kim JK, Rossi NF, Stephenson LW, O’Leary DS. Muscle metaboreflex control of ventricular contractility during dynamic exercise. Am J Physiol Heart Circ Physiol 290: H751-H757, 2006.
63. Sheriff DD, Augstyniak RA, O’Leary DS. Muscle chemoreflex-induced increases in right atrial pressure. Am J Physiol Heart Circ Physiol 275: H767-H775, 1998.
64. Shiki K, Hearse DJ. Preconditioning of ischemic myocardium: reperfusion-induced arrhythmias. Am J Physiol Heart Circ Physiol 253: H1470-H1476, 1987.
65. Shoemaker JK, Mattar L, Kerbeci P, Trotter S, Arbeille P, Hughson RL. WISE 2005: stroke volume changes contribute to the pressor response during ischemic handgrip exercise in women. J Appl Physiol 103: 228-233, 1995.
66. Strange S, Secher NH, Pawelczyk JA, Karpakka J, Christensen NJ, Mitchell JH, Saltin B. Neural control of cardiovascular responses and of ventilation during dynamic exercise in man. J Physiol 470: 693-704, 1993.
67. Tocco F, Marongiu E, Ghiani G, Sanna I, Palazzolo G, Olla S, Pusceddu M, Sanna P, Corona F, Concu A, Crisafulli A. Muscle ischemic preconditioning does not improve performance during self-paced exercise. Int J Sports Med 36: 9-15, 2015.
68. Yellon DM, Downey JM. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83: 1113-1151, 2003.