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Current concepts of oxygen transport during exercise

Published online by Cambridge University Press:  09 March 2007

DC Poole
DC Poole*
Affiliation:
Departments of Kinesiology, Anatomy and Physiology, Kansas State University, Manhattan, KS 66506–5602, USA
*
*[email protected]
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Abstract

This brief review examines the athletic potential of mammals in general and the horse in particular as it relates to oxygen (O2) transport and utilization. The horse has been bred selectively for over six millennia based upon its ability to run fast. Whereas this has optimized cardiovascular and muscle function and the capacity to deliver and utilize O2, it has resulted in lung failure during intense exercise. Horses in their athletic prime are considered and attention is focused on their maximal capacities as related to O2 transport, irrespective of age per se. Following a few comments on the history of O2, this review moves from established principles of O2 transport at the integrative organ level to the microcirculation and the processes and principles that govern O2 offloading, where much remains to be discovered. Four principal questions are addressed: (1) as an athlete, what are the most outstanding physiological characteristics of the horse? (2) what anatomical and physiological capacities facilitate this superlative performance and such prodigious O2 fluxes (i.e. maximal VO2)? (3) do cardiovascular dynamics or intramuscular energetic processes limit VO2 kinetics (i.e. the speed at which VO2 increases at the onset of exercise)? VO2 kinetics determine the size of the O2 deficit and as such represent an important determinant of muscle metabolism and fatigue; and (4) what determines the efficacy of muscle microcirculatory O2 exchange?

Keywords

Horsecardiovascularmuscularoxygen exchangehaemoglobinoxygen uptake kineticsblood flowoxygen diffusion
Type
Research Article
Information
Equine and Comparative Exercise Physiology , Volume 1 , Issue 1 , February 2004 , pp. 5 - 22
Copyright
Copyright © Cambridge University Press 2004

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References

1Dickerson, RE (1978). Chemical evolution and the origin of life. Scientific American 239: 70–86.CrossRefGoogle ScholarPubMed
2Vidal, G (1984). The oldest eukaryotic cells. Scientific American 250: 48–57.CrossRefGoogle ScholarPubMed
3Dickerson, RE (1980). Cytochrome c and the evolution of energy metabolism. Scientific American 242: 137–153.Google Scholar
4Astrand, P-O and Rodahl, K (1986). Textbook of Work Physiology. 3rd ed. New York: McGraw-Hil.Google Scholar
5Valentine, JW (1978). The evolution of multicellular plants and animals. Scientific American 239: 140–146.CrossRefGoogle ScholarPubMed
6West, JB (1980). Historical development. In: West, JB (Ed.) Pulmonary Gas Exchange. Vol. I. New York: Academic Press, pp. 1–32.Google Scholar
7West, JB (1996). Pulmonary blood flow. Respiratory Physiology: People and Ideas. New York: Oxford University Press, pp. 140–169.CrossRefGoogle Scholar
8Lyons, AS and Petrucelli, RJ (1987). Medicine: An Illustrated History. New York: Harry N Abrams Inc, p. 603.Google Scholar
9Pratt, GW (1991). Clocking the fastest horses on earth. The Quarter Racing Journal 4: 36–40.Google Scholar
10Kubo, K (1991). The science for training of Thoroughbred horses. In: Kubo, K (Ed.) The Race Horse. Japan Racing Association, Equine Research Institute, p. 6.Google Scholar
11Jones, JH and Lindstedt, SL (1993). Limits to maximal performance. Annual Review of Physiology 55: 547–569.Google Scholar
12Weibel, ER (1984). The Pathway for Oxygen: Structure and Function in the Mammalian Respiratory System. London: Harvard University Press, pp. 399–404.Google Scholar
13Lindstedt, SL, Hokanson, JF, Wells, DJ, Swain, SD, Hoppeler, H and Navarro, V (1991). Running energetics in the pronghorn antelope. Nature 353: 748–750.CrossRefGoogle ScholarPubMed
14Young, LE, Marlin, DJ, Deaton, C, Brown-Feltner, H, Roberts, CA and Wood, J.L.N. (2002). Heart size estimated by echocardiography correlates with maximal oxygen uptake. Equine Veterinary Journal Supplement 34: 467–471.Google Scholar
15Gunn, HM (1987). Muscle, bone and fat proportions and muscle distribution of Thoroughbreds and other horses. In: Gillespie, JR and Robinson, NE (eds) Equine Exercise Physiology 2. David, CA: ICEEP Publications, pp. 253–264.Google Scholar
16McDonough, P, Kindig, CA, Hildreth, T, Behnke, BJ, Erickson, HH and Poole, DC (2002). Effect of body incline on cardiac performance. Equine Veterinary Journal Supplement 34: 506–509.CrossRefGoogle Scholar
17Stray-Gundersen, J, Musch, TI, Haidet, GC, Swain, DP, Ordway, GA and Mitchell, JH (1986). The effect of pericardiectomy on maximal oxygen consumption and maximal cardiac output in untrained dogs. Circulation Research 58: 523–530.CrossRefGoogle ScholarPubMed
18Hammond, HK, White, FC, Bhargava, V and Shabetai, R (1992). Heart size and maximal cardiac output are limited by the pericardium. American Journal of Physiology 263: H1675–H1681.Google ScholarPubMed
19Wagner, PD (1996). Determinants of maximal oxygen transport and utilization. Annual Review of Physiology 58: 21–50.CrossRefGoogle ScholarPubMed
20Knight, DR, Schaffartzik, W, Poole, DC, Hogan, MC, Bebout, DE and Wagner, PD (1993). Effects of hyperoxia on maximal leg O2 supply and utilization in men. Journal of Applied Physiology 75: 2586–2594.Google Scholar
21Richardson, RS, Poole, DC, Knight, DR, Kurdak, SS, Hogan, MC, Grassi, B, et al. (1993). High muscle blood flow in man: is maximal O2 extraction compromised? Journal of Applied Physiology 75: 1911–1916.CrossRefGoogle Scholar
22Knight, DR, Poole, DC, Schaffartzik, W, Guy, HJ, Prediletto, R, Hogan, MC, et al. (1992). Relationship between body and leg O2 during maximal cycle ergometry. Journal of Applied Physiology 73: 1114–1121.CrossRefGoogle ScholarPubMed
23Gledhill, N (1982). Blood doping and related issues: a brief review. Medicine and Science in Sports and Exercise 14: 183–189.CrossRefGoogle ScholarPubMed
24Wagner, PD, Erickson, BK, Kubo, K, Hiraga, A, Kai, M, Yamana, Y, et al. (1995). Maximum oxygen transport and utilisation before and after splenectomy. Equine Veterinary Journal Supplement 18: 82–85.Google Scholar
25Wagner, PD (1995). Determinants of O2max: man vs. horse. Journal of the Equine Veterinary Society 15: 398–404.Google Scholar
26Wagner, PD, Hoppeler, H and Saltin, B (1997). Determinants of maximal oxygen uptake. In: Crystal, RG, WestJB, JB,, Barnes, PJ and Weibel, ER (eds) The Lung: Scientific Foundations. 2nd ed. New York: Lippincott-Raven, pp. 2033–2041.Google Scholar
27Hoppeler, H and Weibel, ER (1998). Limits for oxygen and substrate transport in mammals. Journal of Experimental Biology 201: 1051–1064.CrossRefGoogle ScholarPubMed
28Grande, F and Taylor, HL (1965). Adaptive changes in the heart, vessels, and patterns of control under chronically high loads. In: Hamilton, WF and Dow, P (eds) Handbook of Physiology. III Section 2. Washington, DC: American Physiological Society, pp. 2616–2621.Google Scholar
29Schoning, P, Erickson, H and Milliken, GA (1995). Body weight, heart weight, and heart-to-body weight ratio in greyhounds. American Journal of Veterinary Research 56: 420–422.Google Scholar
30Haun, M (1997). The X Factor. What It Is and How To Find It. Neenah, WI: Russell Meerdink Co.Google Scholar
31Webb, AI and Weaver, BMQ (1979). Body composition of the horse. Equine Veterinary Journal 11: 39–47.CrossRefGoogle ScholarPubMed
32Evans, DL and Rose, RJ (1988). Cardiovascular and respiratory responses to exercise in thoroughbred horses. Journal of Experimental Biology 134: 397–408.CrossRefGoogle ScholarPubMed
33Persson, SGB, Ekman, L, Lydin, G and Tufvesson, G (1973). Circulatory effects of splenectomy in the horse II. Effect on plasma volume and total and circulating red-cell volume. Zentralblatt für Veterinarmedizin. Reihe A 20: 456–468.Google Scholar
34Moore, J (1994). Nature's supercharger. Equus 198: 30–34.Google Scholar
35Kline, H and Foreman, JH (1991). Heart and spleen weights as a function of breed and somatotype. Equine Exercise Physiology 3: 17–21.Google Scholar
36Erickson, BK, Erickson, HH and Coffman, JR (1990). Pulmonary artery, aortic and oesophageal pressure changes during high-intensity treadmill exercise in the horse: a possible relation to exercise induced pulmonary haemorrhage. Equine Veterinary Journal Supplement 9: 47–52.Google Scholar
37Wagner, PD, Gillespie, JR, Landgren, GL, Fedde, MR, Jones, BW, DeBowes, RM, et al. (1989). Mechanism of exerciseinduced hypoxemia in horses. Journal of Applied Physiology 66: 1227–1233.CrossRefGoogle ScholarPubMed
38Kindig, CA, Gallatin, LL, Erickson, HH, Fedde, MR and Poole, DC (2000). Cardiorespiratory impact of the nitric oxide synthase inhibitor L-NAME in the exercising horse. Respiratory Physiology and Neurobiology 120: 151–166.Google Scholar
39McDonough, P, Kindig, CA, Erickson, HH and Poole, DC (2002). Mechanistic basis for the gas exchange threshold in the Thoroughbred horse. Journal of Applied Physiology 92: 1499–1505.CrossRefGoogle Scholar
40Karas, RH, Taylor, CR, Jones, JH, Lindstedt, SL, Reeves, RB and Weibel, ER (1987). Adaptive variation in the mammalian respiratory system in relation to energetic demand VII. Flow of oxygen across the pulmonary gas exchanger. Respiratory Physiology and Neurobiology 69: 101–115.CrossRefGoogle Scholar
41Constantinopol, M, Jones, JH, Weibel, ER, Taylor, CR, Lindholm, A and Karas, RH (1989). Oxygen transport during exercise in large mammals II. Oxygen uptake by the pulmonary gas exchanger. Journal of Applied Physiology 67: 871–878.Google Scholar
42Gleed, FD, Ducharme, NG, Hackett, RP, Hakim, TS, Erb, HN, Mitchell, LM, et al. (1999). Effects of frusemide on pulmonary capillary pressure in horses exercising on a treadmill. Equine Veterinary Journal Supplement 30: 102–106.Google Scholar
43Sosa Leon, L, Hodgson, DR, Evans, DL, Ray, SP, Carlson, GP and Rose, RJ (2002). Hyperhydration prior to moderate-intensity exercise causes arterial hypoxaemia. Equine Veterinary Journal Supplement 34: 425–429.Google Scholar
44Seaman, J, Erickson, BK, Kubo, K, Hiraga, A, Kai, M, Yamaya, Y, et al. (1995). Exercise-induced ventilation/perfusion inequality in the horse. Equine Veterinary Journal 27: 104–109.Google Scholar
45Marlin, DJ, Scott, CM, Schroter, RC, Harris, RC, Harris, PA, Roberts, CA, et al. (1999). Physiological responses of horses to a treadmill-simulated speed and endurance test in high heat and humidity before and after humid heat acclimation. Equine Veterinary Journal 31: 31–42.CrossRefGoogle ScholarPubMed
46Whipp, BJ and Mahler, M (1980). Dynamics of pulmonary gas exchange during exercise. In: West, JB (Ed.), Pulmonary Gas Exchange. New York: Academic Press, Vol. 2 pp. 33–96.Google Scholar
47Whipp, BJ and Ward, SA (1990). Physiological determinants of pulmonary gas exchange kinetics during exercise. Medicine and Science in Sports and Exercise 22: 62–71.Google Scholar
48Poole, DC and Richardson, RS (1997). Determinants of oxygen uptake: implications for exercise testing. Sports Medicine 24: 308–320.Google Scholar
49Whipp, BJ (1987). Dynamics of pulmonary gas exchange. Circulation 76: VI18–28.Google ScholarPubMed
50Whipp, BJ, Ward, SA, Lamarra, N, Davis, JA and Wasserman, K (1982). Parameters of ventilatory and gas exchange dynamics during exercise. Journal of Applied Physiology 52: 1506–1513.Google Scholar
51Whipp, BJ and Wasserman, K (1972). Oxygen uptake kinetics for various intensities of constant-load work. Journal of Applied Physiology 33: 351–356.CrossRefGoogle ScholarPubMed
52Whipp, BJ and Wasserman, K (1986). Effect of anaerobiosis on the kinetics of O2 uptake during exercise. Federation Proceedings 45: 2942–2947.Google ScholarPubMed
53Barstow, TJ and Mole, PA (1991). Linear and nonlinear characteristics of oxygen uptake kinetics during heavy exercise. Journal of Applied Physiology 71: 2099–2106.Google Scholar
54Paterson, DH and Whipp, BJ (1991). Asymmetries of oxygen uptake transients at the on- and offset of heavy exercise in humans. Journal of Physiology 443: 575–586.Google Scholar
55Langsetmo, I, Weigle, GE, Fedde, MR, Erickson, HH, Barstow, TJ and Poole, DC (1997). O2 kinetics in the horse during moderate and heavy exercise. Journal of Applied Physiology 83: 1235–1241.CrossRefGoogle ScholarPubMed
56Powers, SK, Dodd, S and Beadle, RE (1985). Oxygen uptake kinetics in trained athletes differing in O2max. European Journal of Applied Physiology and Occupational Physiology 54: 306–308.Google Scholar
57Poole, DC (1997). Influence of exercise training on skeletal muscle oxygen delivery and utilization. In: Crystal, RG, West, JB, Weibel, ER, and Barnes, PJ (eds) The Lung: Scientific Foundations. New York: Raven Press, pp. 1957–1967.Google Scholar
58Yoshida, T, Udo, M, Ohmori, T, Matsumoto, Y, Uramoto, T and Yamamoto, K (1992). Day-to-day changes in oxygen uptake kinetics at the onset of exercise during strenuous endurance training. European Journal of Applied Physiology and Occupational Physiology 64: 78–83.CrossRefGoogle ScholarPubMed
59Paterson, DH, Cunningham, DA, Pickering, JG, Babcock, MA and Boughner, DR (1994). Oxygen uptake kinetics in cardiac transplant recipients. Journal of Applied Physiology 77: 1935–1940.CrossRefGoogle ScholarPubMed
60Hepple, RT, Liu, PP, Plyley, MJ and Goodman, JM (1999). Oxygen uptake kinetics during exercise in chronic heart failure: influence of peripheral vascular reserve. Clinical Science (London) 97: 569–577.CrossRefGoogle ScholarPubMed
61Full, RJ and Herreid, CF (1983). Aerobic response to exercise of the fastest land crab. American Journal of Physiology 244: R530–R536.Google Scholar
62Grassi, B, Poole, DC, Richardson, RS, Knight, DR, Erickson, BK and Wagner, PD (1996). Muscle O2 uptake kinetics in humans: implications for metabolic control. Journal of Applied Physiology 80: 988–998.Google Scholar
63Hogan, MC, Gladden, LB, Kurdak, SS and Poole, DC (1995). Increased [lactate] in working dog muscle reduces tension development independent of pH. Medicine and Science in Sports and Exercise 27: 371–377.CrossRefGoogle ScholarPubMed
64Jasperse, JL and Laughlin, MH (1999). Vasomotor responses of soleus feed arteries from sedentary and exercise-trained rats. Journal of Applied Physiology 86: 441–449.CrossRefGoogle ScholarPubMed
65Hughson, RL, Cochrane, JE and Butler, GC (1993). Faster O2 uptake kinetics at onset of supine exercise with, and without, lower body negative pressure. Journal of Applied Physiology 75: 1962–1967.CrossRefGoogle ScholarPubMed
66MacDonald, MJ, Naylor, HL, Tschakovsky, ME and Hughson, RL (2001). Peripheral circulatory factors limit rate of increase in muscle O2 uptake at onset of heavy exercise. Journal of Applied Physiology 90: 83–89.Google Scholar
67Grassi, B (2000). Skeletal muscle O2 on-kinetics: set by O2 delivery or by O2 utilization? New insights into an old issue. Medicine and Science in Sports and Exercise 32: 108–116.Google Scholar
68Grassi, B (2001). Regulation of oxygen consumption at exercise onset: is it really controversial? Exercise and Sport Sciences Reviews 29: 134–138.Google Scholar
69Behnke, BJ, Kindig, CA, Musch, TI, Koga, S and Poole, DC (2001). Dynamics of microvascular oxygen pressure across the rest–exercise transition in rat skeletal muscle. Respiratory Physiology and Neurobiology 126: 53–63.Google Scholar
70Grassi, B, Gladden, LB, Samaja, M, Stary, CM and Hogan, MC (1998). Faster adjustment of O2 delivery does not affect O2 on-kinetics in isolated in situ canine muscle. Journal of Applied Physiology 85: 1394–1403.Google Scholar
71Bangsbo, J, Krustrup, P, Gonzalez-Alonso, J, Boushel, R and Saltin, B (2000). Muscle oxygen kinetics at onset of intense dynamic exercise in humans. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 279: R899–R906.Google Scholar
72Kindig, CA, McDonough, P, Erickson, HH and Poole, DC (2002). Nitric oxide synthase inhibition speeds oxygen uptake kinetics in horses during moderate domain running. Respiratory Physiology and Neurobiology 132: 169–178.Google Scholar
73Kindig, CA, McDonough, P, Erickson, HH and Poole, DC (2001). Effect of L-NAME on oxygen uptake kinetics during heavy-intensity exercise in the horse. Journal of Applied Physiology 91: 891–896.Google Scholar
74Hirai, T, Visneski, MD, Kearns, KJ, Zelis, R and Musch, TI (1994). Effects of NO synthase inhibition on the muscular blood flow response to treadmill exercise in rats. Journal of Applied Physiology 77: 1288–1293.Google Scholar
75Engelen, M, Porszasz, J, Riley, M, Wasserman, K, Maehara, K and Barstow, TJ (1996). Effects of hypoxic hypoxia on O2 uptake and heart rate kinetics during heavy exercise. Journal of Applied Physiology 81: 2500–2508.Google Scholar
76Macdonald, M, Pedersen, PK and Hughson, RL (1997). Acceleration of O2 kinetics in heavy submaximal exercise by hyperoxia and prior high-intensity exercise. Journal of Applied Physiology 83: 1318–1325.Google Scholar
77Rowell, LB (1993). Human Cardiovascular Control. Oxford: Oxford University Press, pp. 255–288.Google Scholar
78Duling, BR and Dora, K (1997). Control of striated muscle blood flow. In: Crystal, RG, West, JB, Weibel, ER, and Barnes, PJ (eds) The Lung: Scientific Foundations. New York: Raven Press, pp. 1935–1943.Google Scholar
79Laughlin, MH, McAllister, RM and Delp, MD (1997). Heterogeneity of blood flow in skeletal muscle. In: Crystal, RG, West, JB, Weibel, ER, and Barnes, PJ (eds) The Lung: Scientific Foundations. New York: Raven Press, pp. 1945–1955.Google Scholar
80Segal, SS (2000). Integration of blood flow control to skeletal muscle: key role of feed arteries. Acta Physiologica Scandinavica 168: 511–518.Google Scholar
81Hornicke, H, von Engelhardt, W and Ehrlein, HJ (1977). Effect of exercise on systemic blood pressure and heart rate in horses. Pflügers Archiv 372: 95–99.CrossRefGoogle ScholarPubMed
82Parks, CM and Manohar, M (1983). Distribution of blood flow during moderate and strenuous exercise in ponies (Equus caballus). American Journal of Veterinary Research 44: 1861–1866.Google Scholar
83Evans, DL (1994). The cardiovascular system: anatomy, physiology, and adaptations to exercise and training. In: Hodgson, DR, and Rose, RJ (eds) The Athletic Horse. Philadelphia, PA: WB Saunders Co, pp. 129–144.Google Scholar
84Laughlin, MH, Korthuis, RJ, Duncker, DJ and Bache, RJ (1996). Control of blood flow to cardiac and skeletal muscle during exercise. In: Rowell, LB, and Shepherd, JT (eds) Handbook of Physiology. New York: Oxford University Press, pp. 705–769.Google Scholar
85Sheriff, DD and Hakeman, AL (2001). Role of speed vs. grade in relation to muscle pump function at locomotion onset. Journal of Applied Physiology 91: 269–276.Google Scholar
86Kindig, CA, Richardson, TE and Poole, DC (2002). Skeletal muscle capillary hemodynamics from rest to contractions: implications for oxygen transfer. Journal of Applied Physiology 92: 2513–2520.Google Scholar
87Manohar, M (1986). Vasodilator reserve in respiratory muscles during maximal exertion in ponies. Journal of Applied Physiology 60: 1571–1577.Google Scholar
88Manohar, M (1988). Costal vs. crural diaphragmatic blood flow during submaximal and near-maximal exercise in ponies. Journal of Applied Physiology 65: 1514–1519.Google Scholar
89Armstrong, RB, Essen-Gustavsson, B, Hoppeler, H, Jones, JH, Kayar, SR, Laughlin, MH, et al. (1992). O2 delivery at O2max and oxidative capacity in muscles of Standardbred horses. Journal of Applied Physiology 73: 2274–2282.Google Scholar
90Popel, AS, Pittman, RN and Ellsworth, ML (1989). Rate of oxygen loss from arterioles is at an order of magnitude higher than expected. American Journal of Physiology 256: H921–H924.Google ScholarPubMed
91Ishikawa, H, Sawada, H and Yamada, E (1983). Surface and internal morphology of skeletal muscle. In: Peachy, LD, Adrian, RH, and Geiger, SR (eds) Handbook of Physiology. Section 10: Skeletal muscle Bethesda, MD: American Physiological Society, pp. 1–22.Google Scholar
92Saltin, B and Gollnick, PD (1983). Skeletal muscle adaptability: significance for metabolism and performance. In: Peachy, LD, Adrian, RH and Geiger, SR (eds) Handbook of Physiology. Section 10: Skeletal muscle Bethesda, MD: American Physiological Society, pp. 555–631.Google Scholar
93Poole, DC and Mathieu-Costello, O (1996). Relationship between fibre capillarization and mitochondrial volume density in control and trained rat soleus and plantaris muscles. Microcirculation 3: 175–186.Google Scholar
94Mathieu-Costello, O, Hoppeler, H and Weibel, ER (1989). Capillary tortuosity in skeletal muscles of mammals depends on muscle contraction. Journal of Applied Physiology 66: 1436–1442.Google Scholar
95Poole, DC, Gaesser, GA, Hogan, MC, Knight, DR and Wagner, PD (1992). Pulmonary and leg O2 during submaximal exercise: implications for muscular efficiency. Journal of Applied Physiology 72: 805–810.Google Scholar
96Delp, MD (1999). Control of skeletal muscle perfusion at the onset of dynamic exercise. Medicine and Science in Sports and Exercise 31: 1011–1018.Google Scholar
97Wunsch, SA, Muller-Delp, J and Delp, MD (2000). Time course of vasodilatory responses in skeletal muscle arterioles: role in hyperemia at onset of exercise. American Journal of Physiology 279: H1715–H1723.Google Scholar
98Berg, BR, Cohen, KD and Sarelius, IH (1997). Direct coupling between blood flow and metabolism at the capillary level in striated muscle. American Journal of Physiology 272: H2693–H2700.Google Scholar
99Musch, TI, McAllister, RM, Symons, JD, Stebbins, CL, Hirai, T, Hageman, KS, et al. (2001). Effects of nitric oxide synthase inhibition on vascular conductance during high-speed treadmill exercise in rats. Experimental Physiology 86: 749–757.Google Scholar
100Federspiel, WJ and Popel, AS (1986). A theoretical analysis of the effect of the particulate nature of blood on oxygen release in capillaries. Microvascular Research 32: 164–189.Google Scholar
101Groebe, K and Thews, G (1990). Calculated intra- and extracellular PO2 gradients in heavily-working red muscle. American Journal of Physiology 259: H84–H92.Google Scholar
102Mathieu, O, Cruz-Orive, LM, Hoppeler, H and Weibel, ER (1983). Estimating length density and quantifying anisotropy in skeletal muscle capillaries. Journal of Microscopy 131: 131–146.Google Scholar
103Ellis, CG, Mathieu-Costello, O, Potter, RF, MacDonald, IC and Groom, AC (1990). Effect of sarcomere length on total capillary length in skeletal muscle: in vivo evidence for longitudinal stretching of capillaries. Microvascular Research 40: 63–72.Google Scholar
104Poole, DC and Mathieu-Costello, O (1992). Capillary and fibre geometry in rat diaphragm perfusion fixed in situ at different sarcomere lengths. Journal of Applied Physiology 73: 151–159.Google Scholar
105Poole, DC, Musch, TI and Kindig, CA (1997). In vivo microvascular structural and functional consequences of muscle length changes. American Journal of Physiology 72: H2107–H2114.Google Scholar
106Schwerzmann, K, Hoppeler, H, Kayar, SR and Weibel, ER (1989). Oxidative capacity of muscle and mitochondria: correlation of physiological, biochemical and morphometric characteristics. Proceedings of the National Academy of Sciences of the United States of America 86: 1583–1587.Google Scholar
107Sarelius, IH and Duling, BR (1982). Direct measurement of microvessel hematocrit, red cell flux, velocity and transit time. American Journal of Physiology 243: H1018–1026.Google Scholar
108Poole, DC and Musch, TI (2000). Pulmonary and peripheral gas exchange during exercise. In: Roca, J, Rodriguez-Roisin, R and Wagner, PD (eds) Pulmonary and Peripheral Gas Exchange in Health and Disease. New York: Plenum Press, pp. 469–523.Google Scholar
109Russell, JA, Kindig, CA, Behnke, BJ, Poole, DC and Musch, TI (2003). Effects of aging on capillary geometry and hemodynamics in rat spinotrapezius muscle. American Journal of Physiology. Heart & Circulatory Physiology 285: H251–H258.Google Scholar
110Wagner, WW (1997). Recruitment of gas exchange vessels. In: Crystal, RG, West, JB, Weibel, ER, and Barnes, PJ (eds) The Lung: Scientific Foundations. New York: Raven Press, pp. 1537–1547.Google Scholar
111Krogh, A (1919). The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissues. Journal of Physiology (London) 52: 409–415.Google Scholar
112Honig, CR, Gayeski, TEJ and Groebe, K (1997). Myoglobin and oxygen gradients. In: Crystal, RG, West, JB, Weibel, ER, and Barnes, PJ (eds) The Lung: Scientific Foundations. New York: Raven Press, pp. 1925–1933.Google Scholar
113Richardson, RS, Noyszewski, EA, Kendrick, KF, Leigh, JS and Wagner, PD (1995). Myoglobin O2 desaturation during exercise: evidence of limited O2 transport. Journal of Clinical Investigation 96: 1916–1926.Google Scholar
114Garry, DJ, Ordway, GA, Lorenz, JN, Radford, NB, Chin, ER, Grange, RW, et al. (1998). Mice without myoglobin. Nature 395: 905–908.Google Scholar
115Bakeeva, LE, Chentsov, YuS and Skulachev, VP (1978). Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle. Biochimica et Biophysica Acta 501: 349–369.Google Scholar
116Knight, PK, Sinha, AK and Rose, RJ (1991). Effects of training intensity on maximum oxygen uptake. In: Persson, SGB, and Jeffcott, LB (eds) Equine Exercise Physiology. Davis, CA: ICEEP Publications, 3: pp. 77–82.Google Scholar
117Evans, DL and Rose, RJ (1988). Cardiovascular and respiratory responses to submaximal exercise training in the Thoroughbred horse. Pflügers Archiv 411: 316–321.Google Scholar
118Eaton, MD, Hodgson, DR, Evans, DL and Rose, RJ (1999). Effects of low- and moderate-intensity training on metabolic responses to exercise in Thoroughbreds. Equine Veterinary Journal Supplement 30: 521–527.Google Scholar
119Katz, LM, Bayly, WM, Roeder, MJ, Kingston, JK, and Hines, MT (2000). Effects of training on oxygen consumption of ponies. American Journal of Veterinary Research 61: 986–991.Google Scholar
120Tyler, CM, Golland, LC, Evans, DL, Hodgson, DR and Rose, RJ (1998). Skeletal muscle adaptations to prolonged training, overtraining and detraining in horses. Pflügers Archiv 436: 391–397.Google Scholar
121Holloszy, JO and Coyle, EF (1984). Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. Journal of Applied Physiology 56: 831–838.Google Scholar
122Thomas, DP, Fregin, GF, Gerber, NH and Ailes, NB (1983). Effects of training on cardiorespiratory function in the horse. American Journal of Physiology 245: R160–R165.Google Scholar
123Betros, CL, McKeever, KH, Kearns, CF and Malinowski, K (2002). Effects of aging and training on maximal heart rate and O2max. Equine Veterinary Journal Supplement 34: 100–105.Google Scholar
124Foreman, JH, Bayly, WM, Grant, BD and Gollnick, PD (1990). Standardized exercise test and daily heart rate responses of Thoroughbreds undergoing conventional race training and detraining. American Journal of Veterinary Research 51: 914–920.Google Scholar
125Piiper, J and Scheid, P (1983). Comparison of diffusion and perfusion limitations in alveolar gas exchange. Respiratory Physiology and Neurobiology 51: 287–290.Google Scholar
126Roca, J, Agusti, AG, Alonso, A, Poole, DC, Viegas, C, Barbera, JA, et al. (1992). Effects of training on muscle O2 transport at O2max. Journal of Applied Physiology 73: 1067–1076.Google Scholar
127Essen-Gustavsson, B, McMiken, D, Karlstrom, K, Lindholm, A, Persson, S and Thornton, J (1989). Muscular adaptation of horses during intensive training and detraining. Equine Veterinary Journal 21: 27–33.Google Scholar
128Serrano, AL, Quiroz-Rothe, E and Rivero, J-LL (2000). Early and long-term changes of equine skeletal muscle in response to endurance training and detraining. Pflügers Archiv 441: 263–274.Google Scholar
129Essen-Gustavsson, B and Lindholm, A (1985). Muscle fibre characteristics of active and inactive Standardbred horses. Equine Veterinary Journal 17: 434–438.Google Scholar
130Guy, PS and Snow, DH (1977). The effect of training and detraining on muscle composition in the horse. Journal of Physiology (London) 269: 33–51.Google Scholar
131Hodgson, DR, Rose, RJ, Dimauro, J and Allen, JR (1986). Effects of training on muscle composition in horses. American Journal of Veterinary Research 47: 12–15.Google Scholar
132Lovell, DK and Rose, RJ (1991). Changes in skeletal muscle composition in response to interval- and high-intensity training. In: Persson, S.G.B., Lindholm, A, and Jeffcot, LB (eds) Equine Exercise Physiology 3. Davis, CA: ICEEP Publications, pp. 215–222.Google Scholar
133McKeever, KH, Schurg, WA, Jarrett, SH and Convertino, VA (1987). Exercise training-induced hypervolemia in the horse. Medicine and Science in Sports and Exercise 19: 21–27.Google Scholar
134McKeever, KH, Scali, R, Geiser, S and Kearns, CF (2002). Plasma aldosterone concentration and renal sodium excretion are altered during the first days of training. Equine Veterinary Journal Supplement 34: 524–531.CrossRefGoogle Scholar
135Freeman, GL and LeWinter, MM (1984). Pericardial adaptations during chronic cardiac dilation in dogs. Circulation Research 54: 294–300.Google Scholar
136Lee, M.-C, LeWinter, MM, Freeman, G, Shabetai, R and Fung, YC (1985). Biaxial mechanical properties of the pericardium in normal and volume overload dogs. American Journal of Physiology 249: H222–H230.Google Scholar
137Kubo, K, Senta, T and Sugimoto, O (1974). Relationship between training and heart in the Thoroughbred racehorse. Experimental Reports of Equine Health Laboratory 11: 87–93.Google Scholar
138Young, LE (1999). Cardiac responses to training in 2-year-old Thoroughbreds: an echocardiographic study. Equine Veterinary Journal Supplement 30: 195–198.Google Scholar
139Saltin, B and Rowell, LB (1980). Functional adaptations to physical activity and inactivity. Federation Proceedings 39: 1506–1513.Google ScholarPubMed
140Griffin, KL, Woodman, CR, Price, EM, Laughlin, MH and Parker, JL (2001). Endothelium-mediated relaxation of porcine collateral-dependent arterioles is improved by exercise training. Circulation 104: 1393–1398.CrossRefGoogle ScholarPubMed
141Lash, JM (1998). Exercise training enhances adrenergic constriction and dilation in the rat spinotrapezius muscle. Journal of Applied Physiology 85: 168–174.CrossRefGoogle ScholarPubMed
142Koller, A, Huang, A, Sun, D and Kaley, G (1995). Exercise training augments flow-dependent dilation in rat skeletal muscle arterioles. Role of endothelial nitric oxide and prostaglandins. Circulation Research 76: 544–550.CrossRefGoogle ScholarPubMed
143VanTeeffelen, JW and Segal, SS (2003). Interaction between sympathetic nerve activation and muscle fibre contraction in resistance vessels of hamster retractor muscle. Journal of Physiology 550: 563–574.CrossRefGoogle ScholarPubMed
144Mathieu-Costello, O, Ellis, CG, Potter, RF, MacDonald, IC and Groom, AC (1991). Muscle capillary-to-fibre perimeter ratio: morphometry. American Journal of Physiology 261: H1617–H1625.Google Scholar
145Hepple, RT, Hogan, MC, Stary, C, Bebout, DE, Mathieu-Costello, O and Wagner, PD (2000). Structural basis of muscle O2 diffusing capacity: evidence from muscle function in situ. Journal of Applied Physiology 88: 560–566.Google Scholar
146Nabors, LK, Baumgartner, WA Jr, Janke, SJ, Rose, JR, Wagner, WW Jr and Capen, RL (2003). Red blood cell orientation in pulmonary capillaries and its effect on gas diffusion. Journal of Applied Physiology 94: 1634–1640.Google Scholar
147Poole, DC, Mathieu-Costello, O and West, JB (1989). Capillary tortuosity in rat soleus muscle is not affected by endurance training. American Journal of Physiology 256: H1110–H1116.Google Scholar
148Rivero, JL, Ruz, MC, Serrano, AL and Diz, AM (1995). Effects of a 3-month endurance training programme on skeletal muscle histochemistry in Andalusian Arabian and Anglo-Arabian horses. Equine Veterinary Journal 27: 51–59.CrossRefGoogle Scholar
149Hogan, MC, Willford, DC, Keipert, PE, Faithfull, NS and Wagner, PD (1992). Increased plasma O2 solubility improves O2 uptake of in situ dog muscle working maximally. Journal of Applied Physiology 73: 2470–2475.Google Scholar
150Hepple, RT, Stary, CM, Kohin, S, Wagner, PD and Hogan, MC (2003). No effect of trans sodium crocetinate on maximal O2 conductance or O2max in moderate hypoxia. Respiratory Physiology and Neurobiology 134: 239–246.CrossRefGoogle ScholarPubMed
151Hoppeler, H, Howald, H, Conley, K, Lindstedt, SL, Claassen, H, Vock, P, et al. (1985). Endurance training in humans: aerobic capacity and structure of skeletal muscle. Journal of Applied Physiology 59: 320–327.Google Scholar