• View in gallery

    Mean stride frequency (A), stride length (B), tidal volume (C), mass-specific alveolar ventilation (A/Mb; D) as a function of treadmill speed, and tidal volume (E) and A/Mb (F) as functions of o2/Mb for 5 highly trained Thoroughbred geldings exercising on a treadmill at a 4% incline (squares), 0% incline (horizontal plane; circles), and 4% decline (triangles). Error bars represent SD. Values in panels C and D were standardized to barometric pressure at sea level (101.3 kPa), body temperature, and gas saturated with water vapor at body temperature; abscissas in panels D and F were standardized to temperature (0°C), barometric pressure at sea level, and dry gas; ordinates in panels D and F were standardized to barometric pressure at sea level, body temperature, and gas saturated with water vapor at body temperature. *Value differs significantly from that for the identical speed at a horizontal plane.

  • View in gallery

    Mean mass-specific O2 consumption (o2/Mb; A) and CO2 production (co2/Mb; B), respiratory exchange ratio (RER; co2/o2; C), HR (D), and mass-specific (/Mb; E) and cardiac SV (SV/Mb; F) as a function of treadmill speed for the horses in Figure 1. See Figure 1 for remainder of key.

  • View in gallery

    Mean Paco2 (A), Pao2 (B), Cao2 (C), Co2 (D), arterial O2 saturation (SaO2; E), and arterial hemoglobin concentration (F) as a function of treadmill speed for the horses in Figure 1. See Figure 1 for remainder of key.

  • View in gallery

    Energy cost (o2 at an incline or decline – o2 at a horizontal plane; A) and fractional energy cost (o2 at an incline or decline/o2 at a horizontal plane at identical speed; B) as a function of treadmill speed for the horses in Figure 1. For both regression analyses pertaining to the downhill plane, the 10 m/s values were excluded. See Figure 1 for remainder of key.

  • 1. Eaton MD, Evans DL, Hodgson DR, et al. Effect of treadmill incline and speed on metabolic rate during exercise in Thoroughbred horses. J Appl Physiol 1995; 79:951957.

    • Search Google Scholar
    • Export Citation
  • 2. Hiraga A, Kai M, Kubo K, et al. The effects of incline on cardiopulmonary function during exercise in the horse. J Equine Sci 1995;6:5560.

    • Search Google Scholar
    • Export Citation
  • 3. McDonough P, Kindig CA, Ramsel C, et al. The effect of treadmill incline on maximal oxygen uptake, gas exchange and the metabolic response to exercise in the horse. Exp Physiol 2002; 87:499506.

    • Search Google Scholar
    • Export Citation
  • 4. Schroter RC, Marlin DJ. Modelling the oxygen cost of transport in competitions over ground of variable slope. Equine Vet J Suppl 2002; 34:397401.

    • Search Google Scholar
    • Export Citation
  • 5. Thornton J, Pagan J, Persson S. The oxygen cost of weight loading and inclined treadmill exercise in the horse. In: Gillespie JR, Robinson NE, eds. Equine exercise physiology 2. Davis, Calif: ICEEP Publications, 1987;206214.

    • Search Google Scholar
    • Export Citation
  • 6. Hoyt DF, Wickler SJ, Garcia SF. Oxygen consumption (VO2) during trotting on a 10% decline. Equine Vet J Suppl 2006; 36:573576.

  • 7. Self ZT, Spence AJ, Wilson AM. Speed and incline during Thoroughbred horse racing: racehorse speed supports a metabolic power constraint to incline running but not to decline running. J Appl Physiol 2012; 113:602607.

    • Search Google Scholar
    • Export Citation
  • 8. Abbott BC, Bigland B, Ritchie JM. The physiological cost of negative work. J Physiol 1952; 117:380390.

  • 9. Minetti AE, Moia C, Roi GS, et al. Energy cost of walking and running at extreme uphill and downhill slopes. J Appl Physiol 2002; 93:10391046.

    • Search Google Scholar
    • Export Citation
  • 10. Margaria R. Sulla fisiologia e specialmente sul consumo energetico della marcia e della corsa a varia velocità ed inclinazione del terreno. Atti Accad Naz Lincei 1938; 7:299368.

    • Search Google Scholar
    • Export Citation
  • 11. Woledge RC, Curtin NA, Homsher E. Energetic aspects of muscle contraction. London: Academic Press, 1985;268271.

  • 12. Higbie EJ, Cureton KJ, Warren GL, et al. Effects of concentric and eccentric training on muscle strength, cross-sectional area, and neural activation. J Appl Physiol 1996; 81:21732181.

    • Search Google Scholar
    • Export Citation
  • 13. Raab JL, Eng P, Waschler RA. Metabolic cost of grade running in dogs. J Appl Physiol 1976; 41:532535.

  • 14. Roig M, Macintyre DL, Eng JJ, et al. Preservation of eccentric strength in older adults: evidence, mechanisms and implications for training and rehabilitation. Exp Gerontol 2010; 45:400409.

    • Search Google Scholar
    • Export Citation
  • 15. Roig M, O'Brien K, Kirk G, et al. The effects of eccentric versus concentric resistance training on muscle strength and mass in healthy adults: a systematic review with meta-analysis. Br J Sports Med 2009; 43:556568.

    • Search Google Scholar
    • Export Citation
  • 16. Roig M, Shadgan B, Reid WD. Eccentric exercise in patients with chronic health conditions: a systematic review. Physiother Can 2008; 60:146160.

    • Search Google Scholar
    • Export Citation
  • 17. Seger JY, Arvidsson B, Thorstensson A. Specific effects of eccentric and concentric training on muscle strength and morphology in humans. Eur J Appl Physiol Occup Physiol 1998; 79:4957.

    • Search Google Scholar
    • Export Citation
  • 18. Seger JY, Thorstensson A. Effects of eccentric versus concentric training on thigh muscle strength and EMG. Int J Sports Med 2005; 26:4552.

    • Search Google Scholar
    • Export Citation
  • 19. Sexton WL, Erickson HH. Effects of treadmill elevation on heart rate, blood lactate concentration and packed cell volume during graded submaximal exercise in ponies. Equine Vet J Suppl 1990; 9:5760.

    • Search Google Scholar
    • Export Citation
  • 20. Zou K, Meador BM, Johnson B, et al. The α(7) β(1)-integrin increases muscle hypertrophy following multiple bouts of eccentric exercise. J Appl Physiol 2011; 111:11341141.

    • Search Google Scholar
    • Export Citation
  • 21. Paradisis GP, Bissas A, Cooke CB. Combined uphill and downhill sprint running training is more efficacious than horizontal. Int J Sports Physiol Perform 2009; 4:229243.

    • Search Google Scholar
    • Export Citation
  • 22. Taylor CR. Relating mechanics and energetics during exercise. Adv Vet Sci Comp Med 1994;38A:181215.

  • 23. Taylor CR, Caldwell SL, Rowntree VJ. Running up and down hills: some consequences of size. Science 1972; 178:10961097.

  • 24. Williams RJ, Nankervis KJ, Colborne GR, et al. Heart rate, net transport cost and stride characteristics of horses exercising at walk and trot on positive and negative gradients. Comp Exerc Physiol 2009; 6:113119.

    • Search Google Scholar
    • Export Citation
  • 25. Jones JH, Longworth KE, Lindholm A, et al. Oxygen transport during exercise in large mammals. I. Adaptive variation in oxygen demand. J Appl Physiol 1989; 67:862870.

    • Search Google Scholar
    • Export Citation
  • 26. Birks EK, Jones JH, Berry JD. Plasma lactate kinetics in exercising horses. In: Persson SGB, Lindholm A, Jeffcott LB, eds. Equine exercise physiology 3. Davis, Calif: ICEEP Publications, 1991;179187.

    • Search Google Scholar
    • Export Citation
  • 27. Fedak MA, Rome L, Seeherman HJ. One-step N2-dilution technique for calibrating open-circuit VO2 measuring systems. J Appl Physiol 1981; 51:772776.

    • Search Google Scholar
    • Export Citation
  • 28. Robert C, Valecte JP, Denoix JM. The effects of treadmill inclination and speed on the activity of two hindlimb muscles in the trotting horse. Equine Vet J 2000; 32:312317.

    • Search Google Scholar
    • Export Citation
  • 29. Bramble DM, Carrier DR. Running and breathing in mammals. Science 1983; 219:251256.

  • 30. Margaria R, Cerretelli P, Aghemo P, et al. Energy cost of running. J Appl Physiol 1963; 18:367370.

  • 31. Pivarnik JM, Sherman NW. Responses of aerobically fit men and women to uphill/downhill walking and slow jogging. Med Sci Sports Exerc 1990; 22:127130.

    • Search Google Scholar
    • Export Citation
  • 32. Minetti AE, Ardig OL, Reinach E, et al. The relationship between mechanical work and energy expenditure of locomotion in horses. J Exp Biol 1999; 202:23292338.

    • Search Google Scholar
    • Export Citation

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Cardiorespiratory function in Thoroughbreds during locomotion on a treadmill at an incline or decline

Hajime Ohmura DVM, PhD1, Kazutaka Mukai DVM, PhD2, Toshiyuki Takahashi DVM, PhD3, Hiroko Aida DVM, PhD4, and James H. Jones DVM, PhD5
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  • 1 Sports Science Division, Equine Research Institute, Japan Racing Association, 321-4 Tokami-cho, Utsunomiya-shi, Tochigi 320-0856 Japan.
  • | 2 Sports Science Division, Equine Research Institute, Japan Racing Association, 321-4 Tokami-cho, Utsunomiya-shi, Tochigi 320-0856 Japan.
  • | 3 Sports Science Division, Equine Research Institute, Japan Racing Association, 321-4 Tokami-cho, Utsunomiya-shi, Tochigi 320-0856 Japan.
  • | 4 Sports Science Division, Equine Research Institute, Japan Racing Association, 321-4 Tokami-cho, Utsunomiya-shi, Tochigi 320-0856 Japan.
  • | 5 Department of Surgical & Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

Abstract

OBJECTIVE To determine cardiorespiratory responses of Thoroughbreds to uphill and downhill locomotion on a treadmill at identical gradients.

ANIMALS 5 highly trained Thoroughbred geldings.

PROCEDURES Thoroughbreds were exercised for 2-minute intervals on a treadmill at 1.7, 3.5, 6.0, 8.0, and 10.0 m/s at a 4% incline, 0% incline (horizontal plane), and 4% decline in random order on different days. Stride frequency, stride length, and cardiopulmonary and O2-transport variables were measured and analyzed by means of repeated-measures ANOVA and Holm-Šidák pairwise comparisons.

RESULTS Horses completed all treadmill exercises with identical stride frequency and stride length. At identical uphill speeds, they had higher (vs horizontal) mass-specific O2 consumption (mean increase, 49%) and CO2 production (mean increase, 47%), cardiac output (mean increase, 21%), heart rate (mean increase, 11%), and Paco2 (mean increase, 1.7 mm Hg), and lower Pao2 (mean decrease, 5.8 mm Hg) and arterial O2 saturation (mean decrease, 1.0%); tidal volume was not higher. Downhill locomotion (vs horizontal) reduced mass-specific O2 consumption (mean decrease, 24%), CO2 production (mean decrease, 23%), and cardiac output (mean decrease, 9%). Absolute energy cost during uphill locomotion increased linearly with speed at approximately twice the rate at which it decreased during downhill locomotion.

CONCLUSIONS AND CLINICAL RELEVANCE Findings suggested that for Thoroughbreds, downhill locomotion resulted in a lower energy cost than did horizontal or uphill locomotion and that this cost changed with speed. Whether eccentric training induces skeletal muscle changes in horses similar to those in humans remains to be determined.

Abstract

OBJECTIVE To determine cardiorespiratory responses of Thoroughbreds to uphill and downhill locomotion on a treadmill at identical gradients.

ANIMALS 5 highly trained Thoroughbred geldings.

PROCEDURES Thoroughbreds were exercised for 2-minute intervals on a treadmill at 1.7, 3.5, 6.0, 8.0, and 10.0 m/s at a 4% incline, 0% incline (horizontal plane), and 4% decline in random order on different days. Stride frequency, stride length, and cardiopulmonary and O2-transport variables were measured and analyzed by means of repeated-measures ANOVA and Holm-Šidák pairwise comparisons.

RESULTS Horses completed all treadmill exercises with identical stride frequency and stride length. At identical uphill speeds, they had higher (vs horizontal) mass-specific O2 consumption (mean increase, 49%) and CO2 production (mean increase, 47%), cardiac output (mean increase, 21%), heart rate (mean increase, 11%), and Paco2 (mean increase, 1.7 mm Hg), and lower Pao2 (mean decrease, 5.8 mm Hg) and arterial O2 saturation (mean decrease, 1.0%); tidal volume was not higher. Downhill locomotion (vs horizontal) reduced mass-specific O2 consumption (mean decrease, 24%), CO2 production (mean decrease, 23%), and cardiac output (mean decrease, 9%). Absolute energy cost during uphill locomotion increased linearly with speed at approximately twice the rate at which it decreased during downhill locomotion.

CONCLUSIONS AND CLINICAL RELEVANCE Findings suggested that for Thoroughbreds, downhill locomotion resulted in a lower energy cost than did horizontal or uphill locomotion and that this cost changed with speed. Whether eccentric training induces skeletal muscle changes in horses similar to those in humans remains to be determined.

Race horses train on various surfaces, including dirt, turf, wood chips, and all-weather synthetic materials. A method commonly used to enhance cardiovascular fitness in horses is to train them by having them run uphill. Several investigators have measured or modeled the relationship between uphill running and energy expenditure, HR, and o2.1–5 However, few reports6,7 exist regarding the effects of downhill locomotion on horses.

Downhill locomotion requires that muscles perform eccentric contractions (ie, do negative work), during which the muscles generate tension even as they are lengthening. Because efficiency is defined as metabolic power input divided by mechanical power output, eccentric contractions enable skeletal muscle to contract with a larger magnitude efficiency (approx −1.20 on slopes exceeding a 20% decline)8,9 than for concentric contractions (approx 0.25 on slopes exceeding a 20% incline).10,11 Eccentric muscle contractions affect human skeletal muscle differently than concentric contractions, increasing muscle size and strength more than concentric exercise training and with reduced o2.4,12–20 Some human athletes train by running downhill to increase their running speed.21 The additional potential energy available during downhill running may translate into faster fibers that can accelerate the speed of horizontal running.21 However, during horse racing, Thoroughbreds reportedly run slower than on horizontal surfaces, not only when going uphill but also going downhill.7 In addition, larger animals have a greater difference in energy cost than do smaller animals when running uphill, downhill, and horizontally.22,23

A better understanding of the skeletal muscle and cardiopulmonary responses to downhill running may suggest a beneficial role for downhill running in Thoroughbred training. To our knowledge, only 1 study24 has been conducted to evaluate the effects on energetics and O2 transport in the same group of horses during locomotion uphill and downhill at equivalent gradients. We hypothesized that locomotion of Thoroughbreds on a treadmill at a decline would result in a lower metabolic energy cost and reduced cardiopulmonary function, compared with locomotion at equivalent speed on a treadmill at a horizontal plane. Furthermore, we hypothesized that the reduction in those energy costs going downhill would equal the increase in energy costs when going uphill against gravity. Restated, we hypothesized that the difference in work done in raising a Thoroughbred's Mb against gravity going uphill and saved when going downhill would be equal and result in metabolic power changes of equal magnitude.

Materials and Methods

Ethics statement

Protocols for the study were reviewed and approved by the Animal Welfare and Ethics Committee of the Japan Racing Association.

Animals

Five highly trained Thoroughbred geldings from the Japan Racing Association's Equine Research Institute herd (mean ± SD body weight, 439 ± 22 kg; mean age, 3.8 ± 1.8 years) were used in the study. The horses had undergone a preliminary surgery at 1 or 2 years of age to move a carotid artery from the carotid sheath to a subcutaneous location to facilitate arterial catheterization. Horses were exercised 5 d/wk on a treadmilla for a period of 2 months before the study began. At that time, the horses achieved reproducible maximum mass-specific rates of O2 consumption (o2/Mb) of 154 ± 13 mL of O2/kg•min.

Treadmill exercises

Horses were exercised on a treadmill for data collection once per week at 1 of 3 gradients that were assigned in random order (ie, by use of a random number generator) for measurement of O2-transport variables at various exercise intensities. Before horses were led onto the treadmill, an 18-gauge, 6.4-cm catheterb was placed in a carotid artery and an 8.5F, 9-cm introducerc was placed in a jugular vein. A Swan-Ganz catheterd was passed via the jugular introducer so that its tip was positioned in the pulmonary artery; this position was confirmed by measuring the pressure waveform at its tip with a pressure transducer.e The Swan-Ganz catheter was used to collect samples of mixed-venous (pulmonary arterial) blood, and its thermistor was used to measure blood temperature for correction of blood gas data. A surcingle with ECG electrodes was placed around the thorax of each horse to measure HR with a commercial HR monitor.f

Exercise protocol

After catheters and transducers were connected and tested, each horse began warm-up exercises with 2 minutes of walking (1.7 m/s) and 3 minutes of trotting (3.5 m/s). Horses then exercised for 2-minute incremental intervals on the treadmill at progressive speeds of 1.7 (walk), 3.5 (trot), 6.0 (canter), 8.0 (canter), and 10.0 (canter) m/s at a 4% incline, 0% incline (horizontal plane), or 4% decline in random order on different days; on a given day, horses were exercised at only one of these grades. During these exercises, a semiopen flow mask was placed over the muzzle of each horse for measurement of o2.

Blood sample collection

Horses were exercised at each speed for 90 seconds to achieve a steady state of O2 transport, then during the final 30 seconds at each speed, arterial and mixed-venous blood samples were collected simultaneously for measurement of O2 saturation, O2 concentration, and blood hemoglobin concentration by use of a hemoximeter set to its equine algorithm.g Blood samples were centrifugedh for 5 minutes at 12,000 × g to measure PCV as well as for 5 minutes at 1,800 × g to separate plasma for measurement of plasma lactate concentration with a lactate analyzer.i In conjunction with o2 measured by the semiopen flow system, was calculated by use of the Fick Principle and cardiac SV was calculated as divided by HR.

Mask system and O2 consumption

The mask that horses wore was made of a T-shaped piece of lightweight 20-cm-diameter rigid polyvinylchloride tubing connected to flexible 20-cm-diameter polyvinylchloride tubing on the 2 side arms of the T. On the center tube of the mask, a foam and rubber diaphragm and gasket was mounted that fit around and over the muzzle of the horse and, when taped to the muzzle, formed a gas-tight seal. Ropes passed through overhead pulleys, and elastic cords were attached to the ceiling to support the weight of the mask. All joints in the flow system upstream of the gas analyzers were sealed with duct tape. Air flowed through 20-cm-diameter wire-reinforced flexible tubing affixed to the upstream and downstream ends of the mask and across two 25-cm-diameter pneumotachometersj located equidistant from the mask that were connected to differential pressure transducers.k These were used to ensure that bias flows during measurements were identical to those during calibrations as well as to measure tidal volume and ventilatory frequency.

Oxygen consumption and co2 were measured with standard mass-balance techniques25,26 by use of an O2 and CO2 analyzer,l 2-m-long drying tubem with countercurrent dry-gas flow (anhydrous CaSO4) to remove water from sample gas, and mass flowmetersn for measuring N2 and CO2 calibration flows by means of the N2-dilution, CO2-addition technique.27 Values were standardized to standard temperature (0°C), barometric pressure at sea level (101.3 kPa), and dry gas. Gas analyzer, flowmeter, and pneumotachometer outputs were recorded with an analog-to-digital conversion cardo and softwarep on a personal computer.

Tidal volume and alveolar ventilation

Tidal volume was calculated as the mean difference between the integrated flows through the upstream and downstream pneumotachometers over 10 breaths measured during the final 30 seconds at each speed. Values were standardized to body temperature, barometric pressure, and gas saturated with water vapor at body temperature. Alveolar ventilation was calculated as the ratio of co2 and alveolar CO2 fraction, which in turn was calculated as Paco2 divided by the alveolar dry gas pressure.

Stride frequency and stride length

Video recordings of each exercise session were used to manually count stride frequency. Stride length was calculated as speed divided by stride frequency.

Energy cost

Energy cost of locomotion (COT, or the energy required to transport 1 kg of Mb 1 m of distance) was estimated by fitting linear regressions to the o2 versus speed relationship for each treadmill grade. The effects of grade on relative energy cost of locomotion (ratio of o2 at the 4% incline or 4% decline vs o2 at an identical speed at the horizontal plane for each horse) were calculated for all speeds.

Statistical analysis

Statistical softwareq was used for all data analyses; results are reported as mean ± SD. Two-way repeated measures ANOVA controlling for horse was used to test for differences among treadmill grades and speeds. The Holm-Šidák procedure was used to perform post hoc pairwise comparisons. Most data were normally distributed and homoscedastic; data that were nonnormally distributed were transformed with logarithmic or square-root transformations as required to achieve a normal distribution. Least squares linear regression was used to fit linear data, and ANCOVA was performed to test for differences in regression slopes among the horizontal plane, 4% incline, and 4% decline. Values of P ≤ 0.05 were considered significant.

Results

None of the horses had signs of lameness or muscle soreness after the treadmill exercises. Horses reached their highest o2 when going uphill at 10 m/s, at which time the maximal o2 (mean ± SD, 81.3 ± 12.0 mL of O2/kg•min) was reached. All horses finished exercises at all treadmill grades with plasma lactate concentrations < 6mM, except for 1 horse, in which the concentration was 2.9mM after exercising at the 4% incline at 8 m/s and 19.1mM after exercising for 2 minutes at the same incline at 10 m/s. That horse had an unremarkable maximal o2, and review of the video recording obtained while it exercised revealed no evidence of unusual gait or other external signs of fatigue, so the possibility could not be ruled out that that datum had been recorded erroneously.

Values of all measured variables differed significantly with speed. Horses moved with identical stride frequency and stride length at all treadmill grades (P > 0.70; Figure 1). Tidal volume was not higher when going uphill (P = 0.06), although statistical power was low (0.45), so that finding should be interpreted with caution. For tidal volume, no interaction was identified between treadmill speed and grade (P > 0.23), although for mass-specific alveolar ventilation, such an interaction was identified (P = 0.01).

Figure 1—
Figure 1—

Mean stride frequency (A), stride length (B), tidal volume (C), mass-specific alveolar ventilation (A/Mb; D) as a function of treadmill speed, and tidal volume (E) and A/Mb (F) as functions of o2/Mb for 5 highly trained Thoroughbred geldings exercising on a treadmill at a 4% incline (squares), 0% incline (horizontal plane; circles), and 4% decline (triangles). Error bars represent SD. Values in panels C and D were standardized to barometric pressure at sea level (101.3 kPa), body temperature, and gas saturated with water vapor at body temperature; abscissas in panels D and F were standardized to temperature (0°C), barometric pressure at sea level, and dry gas; ordinates in panels D and F were standardized to barometric pressure at sea level, body temperature, and gas saturated with water vapor at body temperature. *Value differs significantly from that for the identical speed at a horizontal plane.

Citation: American Journal of Veterinary Research 78, 3; 10.2460/ajvr.78.3.340

At identical uphill speeds, horses had a higher mass-specific o2 (mean increase, 49%; P < 0.001), co2 (mean increase, 47%; P < 0.001), and (mean increase, 21%; P < 0.001) and a higher HR (mean increase, 11%; P = 0.04) than at identical horizontal speeds (Figure 2). Downhill (vs horizontal) locomotion resulted in reductions in mass-specific o2 (mean decrease, 24%; P = 0.04), co2 (mean decrease, 23%; P = 0.002), and (mean decrease, 9%; P = 0.03) but had no significant (P = 0.39) effect on HR. Neither respiratory exchange ratio (co2/ o2) nor mass-specific SV changed with treadmill grade, and neither variable had a speed-by-grade interaction (P > 0.30).

Figure 2—
Figure 2—

Mean mass-specific O2 consumption (o2/Mb; A) and CO2 production (co2/Mb; B), respiratory exchange ratio (RER; co2/o2; C), HR (D), and mass-specific (/Mb; E) and cardiac SV (SV/Mb; F) as a function of treadmill speed for the horses in Figure 1. See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 78, 3; 10.2460/ajvr.78.3.340

At identical uphill speeds, horses had a higher Paco2 (mean increase, 1.7 mm Hg), lower Pao2 (mean decrease, 5.8 mm Hg), lower saturation of arterial hemoglobin with O2 (mean decrease, 1.0%), and lower Co2 (mean decrease, 2.3 mL of O2/dL) than at identical horizontal speeds (Figure 3). Downhill (vs horizontal) locomotion resulted in increased Co2 (mean increase, 1.2 mL of O2/dL), although Cao2 did not differ from at the horizontal grade when horses went uphill or downhill. Blood hemoglobin concentration and PCV (data not shown) had a speed-by-grade interaction, with higher values at higher speeds and at the 4% incline.

Figure 3—
Figure 3—

Mean Paco2 (A), Pao2 (B), Cao2 (C), Co2 (D), arterial O2 saturation (SaO2; E), and arterial hemoglobin concentration (F) as a function of treadmill speed for the horses in Figure 1. See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 78, 3; 10.2460/ajvr.78.3.340

Linear regression of mass-specific o2 versus speed (m/s) yielded the following equations for energy COT: for the 4% incline, COT = 0.202 × −0.044 mL of O2/kg•m (R2 = 0.94); for the horizontal plane, COT = 0.152 × −0.096 mL of O2/kg•m (R2 = 0.89); and for the 4% decline, COT = 0.144 × −0.196 mL of O2/kg•m (R2 = 0.87; Figure 4). The ANCOVA revealed that the slope of the regression line for the 4% incline was significantly (P < 0.001) greater than that for the horizontal plane; the slope for the 4% decline was not significantly (P > 0.60) different from that of the horizontal plane, although the intercept in the regression equation for the 4% decline was significantly (P < 0.01) lower than that for the horizontal plane.

Figure 4—
Figure 4—

Energy cost (o2 at an incline or decline – o2 at a horizontal plane; A) and fractional energy cost (o2 at an incline or decline/o2 at a horizontal plane at identical speed; B) as a function of treadmill speed for the horses in Figure 1. For both regression analyses pertaining to the downhill plane, the 10 m/s values were excluded. See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 78, 3; 10.2460/ajvr.78.3.340

The absolute energy cost for uphill versus horizontal locomotion was a mean ± SD of 1.49 ± 0.12 times as great, and that for downhill versus horizontal locomotion was a mean of 0.76 ± 0.11 times as great. When expressed as energy cost difference from that for horizontal locomotion as a function of speed, the linear regression equation for the 4% incline had a slope of 0.0502 mL of O2/kg•m (R2 = 0.50) and that for the 4% decline had a slope of −0.0216 mL of O2/kg•m (R2 = 0.35; Figure 4). We fit the regression equation for the 4% decline data to all 5 data points (speeds) as well as to only the 4 lower speeds, excluding the 10 m/s speed, because the data for mass-specific o2 from which these values were calculated had high variance (Figure 2), and inclusion of the 10 m/s data point in the regression equation reduced the coefficient of determination (R2) by 500% and rendered the regression equation nonsignificant, suggesting that the 10 m/s data point might be an outlier. The fractional energy cost for uphill versus horizontal locomotion as a function of speed did not differ significantly (P = 0.10), and this might have been influenced by the high variance associated with some of the individual data points, although that for downhill versus horizontal locomotion differed significantly (slope = 0.23; R2 = 0.24; P < 0.03).

Discussion

In the study reported here, changes in cardiopulmonary function induced by uphill and downhill locomotion of Thoroughbreds were compared with those induced by horizontal locomotion as a preliminary step in determining whether downhill training might be useful in horses. Direct comparison of our results with those of previous studies is complicated by the fact that only 1 other study24 has been reported that involved direct assessment of the effects of both uphill and downhill (identical gradients) locomotion on energetics and cardiorespiratory function in horses. In that study,24 horses were evaluated only while walking and trotting; O2 consumption was not measured directly but, rather, was extrapolated from HR to estimate COT; and the investigation was partially focused on effects of treadmill grade on kinematics. In addition, other studies of horses have involved uphill1–5 or downhill6,7 locomotion at various gradients. Findings in humans indicate that reductions in energy cost during downhill locomotion are reversed at extremely steep downhill gradients,9 and the same might also be true in horses. Furthermore, because body size markedly affects relative energy cost of locomotion at various gradients, comparison of findings for horses with those for other species is difficult.22,23 Nevertheless, some comparisons can be made with the results of other studies despite these constraints.

Horses in the present study were able to complete all treadmill exercises at all treadmill grades at the same speed with identical stride frequency and stride length (Figure 1). This finding contrasts with that of another study6 in which stride frequency during locomotion at a much steeper downhill gradient (10% decline) was a mean of 2.7% lower than during horizontal locomotion when horses trotted at speeds between 2.25 and 4.0 m/s.r Values of P in the present study for comparisons among treadmill grades were 0.80 and 0.67 for stride frequency and stride length, respectively, and the statistical power for those comparisons was > 0.80, so we were fairly confident that there was indeed no difference among grades when 4% gradients were compared. The steeper downhill gradient (10%) used in the other study6 might have been responsible for the aforementioned difference in study results. However, similar to our findings, another study24 revealed that when stride characteristics were evaluated during locomotion on downhill gradients, no differences were identified in stride frequency or stride length during walking or trotting between downhill and horizontal locomotion. In that study,24 investigators noticed a pattern toward higher stride frequencies when horses walked or trotted uphill, although they did not state whether this pattern was significant and the horses were evaluated at a more limited range of speeds than in the present study. In contrast, other investigators1,2,28 have found that horses have no change in stride frequency or stride length during locomotion at 2.5% to 10% inclines, similar to our findings.

Tidal volume could not be accurately measured in walking horses in the present study because of low ventilatory flows for integration, coupled with the fact that ventilatory frequency was not coupled with stride frequency, so the variance was large. In some horses, ventilation was coupled with stride while trotting, but not in other horses, contributing to the high variance shown for tidal volumes while trotting (Figure 1). In some horses, ventilation was coupled with stride while cantering and galloping, presumably because of locomotor-respiratory coupling due to the visceral piston mechanism.29 Tidal volume appeared to increase at all speeds going uphill; however, when tidal volume was plotted as a function of mass-specific o2, no difference in slopes of the ANCOVA regression lines was detected among treadmill grades.

Mass-specific alveolar ventilation was higher with uphill versus horizontal locomotion at all speeds and was lower with downhill versus horizontal locomotion at all cantering and galloping speeds (Figure 1). However, as with tidal volume, when mass-specific alveolar ventilation was plotted as a function of mass-specific o2 for each treadmill gradient, ANCOVA revealed no difference in slopes of the corresponding regression lines.

At identical uphill speeds versus horizontal speeds, horses had higher mass-specific o2 and co2 (Figure 2). Many studies have revealed that o2 increases linearly with speed and incline1,5,12,13,19,23,30 as it did in the present study and that it increases in direct proportion to the weight carried during uphill running.5 During locomotion at a 4% incline in the present study, the mean mass-specific o2 increased by 49% and co2 by 47%, relative to values during locomotion on a horizontal plane. During locomotion at a 4% decline, the mean mass-specific o2 decreased by 24% and co2 by 23%, relative to values during locomotion on a horizontal plane, in agreement with findings of human studies,9,30 but this was only half of the 45% decrease measured when horses trotted downhill at a 10% gradient in another study.6 The increase in mass-specific o2 during uphill locomotion in the present study was twice as high as the decrease during downhill locomotion, refuting our hypothesis that these 2 differences would be equivalent.

Respiratory exchange ratio (co2/o2) in the present study increased with speed but not with increasing gradient, approaching a value of 1.0 at 10 m/s at a 4% incline (Figure 2). The magnitudes of the values measured could not be directly compared with those in other studies22,23 because of differences in the gradients used as well as the previously mentioned effect of body size on responses.

Heart rate increased with speed and uphill locomotion but did not decrease with downhill locomotion (Figure 2), differing from the results of a study24 in which horses were evaluated while walking and trotting uphill and downhill. Although that study24 revealed linear increases in HR with positive gradients, it also revealed decreases in HR with negative gradients. No HR was reported for horses trotting at a 10% decline.6 In the present study, the mass-specific also increased with uphill locomotion, similar to findings of other studies1,2,5 involving horses. Mass-specific SV increased slightly (16%) only as a function of speed, in contrast with the findings of a previous study2 in which no change in SV was identified with speed or incline.

Horses were typically observed to hyperventilate slightly at most speeds and to only minimally hyperventilate during locomotion at the fastest speeds during downhill or horizontal locomotion in the study reported here; however, marked hypoventilation was detected at the highest speed during uphill locomotion (Paco2 > 52 mm Hg; Figure 3). In association with this hypoventilation, horses were generally observed to become more hypoxemic (Pao2 < 82 mm Hg) as speed increased during uphill locomotion than they were during downhill or horizontal locomotion and had a decrease in arterial O2 saturation (< 94%) at the highest speed. This was a greater degree of hypoventilation than was observed during locomotion at 10.4 m/s and a 3% incline in another study2 (mean ± SD Paco2, 47.5 ± 4.9 mm Hg)s and was associated with mild hypoxemia (85.7 ± 7.4 mm Hg) similar to that identified in the present study.

The increase in arterial hemoglobin concentration with speed and a speed-by-grade interaction resulted in Cao2 increasing with speed independently of treadmill grade (Figure 3), whereas, for Co2, a marked speed-by-grade interaction was identified that reflected the changes in o2 with speed and grade. Our findings that Cao2 increased with speed independently of treadmill grade but that Co2 decreased with speed and grade were similar to findings in another report2 and explained the mechanism by which the arteriovenous CO2 difference increases and greater O2 extraction occurs.

As speed increased, the absolute energy cost (o2) for uphill locomotion increased relative to that of horizontal locomotion, whereas energy cost for downhill locomotion decreased (Figure 4). The slope of the regression line for the COT of locomotion up a 4% incline (0.202) was similar to that previously estimated for locomotion up a 4% incline (0.185),4 3% incline (0.192),2 and 5% incline (0.19).1 All of these estimates of mass-specific o2 are within 12% of the value we estimated for locomotion at 10 m/s up a 4% incline. However, an uphill-downhill energy cost model4 estimate of mass-specific o2 for horses running down a 4% decline at 10 m/s was only 44% of the value measured in the present study, although our measured value may have been biased toward a high number given that all the other data points along the associated regression line were nearly collinear (Figure 4). Nevertheless, our observation that COT increased at twice the rate during uphill versus downhill locomotion was in agreement with measurements in humans31 and similar estimates of COT for horses while walking and trotting.24 The study of walking and trotting horses24 revealed that the COT indirectly estimated from HR during walking uphill at 3% and 6% inclines increased by 30% and 48%, respectively, relative to the COT during horizontal locomotion, and while trotting by 29% and 46%, respectively. With negative gradients, COT decreased relative to the COT of horizontal locomotion while walking at 3% and 6% declines by 20% and 33% and while trotting at these same downhill gradients by 17% and 24%.24 The magnitudes of these differences are similar to those measured in the present study.

When these differences in energy cost were expressed as a fraction of the energy cost for horizontal locomotion, the fractional changes for uphill locomotion did not have a significant linear relationship, although the fractional changes for downhill locomotion did (Figure 4); again, these findings must be interpreted with caution because of the large variance associated with some of the data. These observations may suggest that energy costs and savings due to gravitational forces do not act symmetrically during uphill versus downhill locomotion of horses and that, at least at the modest gradients evaluated (± 4%), differences in energy cost were not strictly attributable to differences between the energy required to raise the center of mass and the potential energy recovered when it was lowered. Nevertheless, these differences in energy cost of horses during uphill and downhill locomotion at identical gradients may provide some insight into the suggestion that the energy cost of locomotion in horses may be set by a combination of the cost of generating force and the cost of producing mechanical work.32 The observation that racing Thoroughbreds run at slower speeds going downhill than on a horizontal surface may be due to the anatomic simplicity of their forelimbs being unable to provide support and stability during downhill running.7 If this were true, then downhill training might be unlikely to improve racing performance of horses, although the effects on muscle function of long-term training with eccentric muscle contractions in horses are unknown and remain to be evaluated.

We hypothesized that Thoroughbreds would have a decrease in metabolic energy cost and cardiopulmonary function during downhill versus horizontal locomotion at equivalent speed on a treadmill and that the cost would increase by an equal and opposite amount during uphill versus horizontal locomotion, while working against gravity. Although some of our data had high variance so that the associated results should be interpreted with caution, downhill locomotion resulted in a lower energy cost than uphill or horizontal locomotion and this cost changed linearly with speed. However, the reduction in o2 during downhill locomotion at a −4% gradient was only approximately half the increased o2 required for uphill locomotion at an equivalent +4% gradient, indicating that not all of the energy difference was simply attributable to gravitational effects. Eccentric contractions occurring during downhill locomotion might contribute to this disparity. Future studies should include assessment of the effects of eccentric muscle contractions on muscle ultrastructure and function. Whether eccentric training will induce skeletal muscle changes in horses similar to those in humans remains to be determined.

Acknowledgments

Supported by the Equine Research Institute, Japan Racing Association, Tochigi, Japan.

Presented as an abstract and poster at the 9th International Conference on Equine Exercise Physiology, Chester, England, June 2014.

ABBREVIATIONS

Cao2

Arterial oxygen concentration

COT

Cost of transport

Co2

Mixed-venous oxygen concentration

HR

Heart rate

Mb

Body mass

Cardiac output

SV

Stroke volume

o2

Rate of metabolic oxygen consumption

co2

Rate of metabolic carbon dioxide production

Footnotes

a.

Säto I, Säto AB, Knivsta, Sweden.

b.

Surflow, Terumo Corp, Tokyo, Japan.

c.

MO95H-8.5, Baxter, Tokyo, Japan.

d.

Criticath, Ohmeda, Madison, Wis.

e.

Statham P23d, Viggo-Spectramed, Tokyo, Japan.

f.

S810, Polar Electro Oy, Kempele, Finland.

g.

OSM3 hemoximeter, Radiometer-Copenhagen, Brønshøj, Denmark.

h.

KH120A, Kubota, Tokyo, Japan.

i.

Biosen C-line glucose lactate analyser, EKF-diagnostic GmbH, Barleben, Germany.

j.

LF-150B, G. N. Sensor, Chiba, Japan.

k.

TF-105, G. N. Sensor, Chiba, Japan.

l.

METS-900, VISE Medical, Chiba, Japan.

m.

Nafion drying tube, Perma Pure LLC, Lakewood, NJ.

n.

Model DPM3, Kofloc, Tokyo, Japan.

o.

DI-720-USB, DATAQ Instruments, Akron, Ohio.

p.

Windaq Pro+, DATAQ Instruments, Akron, Ohio.

q.

SigmaPlot 12.5, Systat, Chicago, Ill.

r.

Hoyt DF, California State Polytechnic University, Pomona, Calif: Personal communication, 2016.

s.

Hiraga A, Japan Racing Association Hidaka Research and Training Center, Hokkaido, Japan: Personal communication, 2016.

References

  • 1. Eaton MD, Evans DL, Hodgson DR, et al. Effect of treadmill incline and speed on metabolic rate during exercise in Thoroughbred horses. J Appl Physiol 1995; 79:951957.

    • Search Google Scholar
    • Export Citation
  • 2. Hiraga A, Kai M, Kubo K, et al. The effects of incline on cardiopulmonary function during exercise in the horse. J Equine Sci 1995;6:5560.

    • Search Google Scholar
    • Export Citation
  • 3. McDonough P, Kindig CA, Ramsel C, et al. The effect of treadmill incline on maximal oxygen uptake, gas exchange and the metabolic response to exercise in the horse. Exp Physiol 2002; 87:499506.

    • Search Google Scholar
    • Export Citation
  • 4. Schroter RC, Marlin DJ. Modelling the oxygen cost of transport in competitions over ground of variable slope. Equine Vet J Suppl 2002; 34:397401.

    • Search Google Scholar
    • Export Citation
  • 5. Thornton J, Pagan J, Persson S. The oxygen cost of weight loading and inclined treadmill exercise in the horse. In: Gillespie JR, Robinson NE, eds. Equine exercise physiology 2. Davis, Calif: ICEEP Publications, 1987;206214.

    • Search Google Scholar
    • Export Citation
  • 6. Hoyt DF, Wickler SJ, Garcia SF. Oxygen consumption (VO2) during trotting on a 10% decline. Equine Vet J Suppl 2006; 36:573576.

  • 7. Self ZT, Spence AJ, Wilson AM. Speed and incline during Thoroughbred horse racing: racehorse speed supports a metabolic power constraint to incline running but not to decline running. J Appl Physiol 2012; 113:602607.

    • Search Google Scholar
    • Export Citation
  • 8. Abbott BC, Bigland B, Ritchie JM. The physiological cost of negative work. J Physiol 1952; 117:380390.

  • 9. Minetti AE, Moia C, Roi GS, et al. Energy cost of walking and running at extreme uphill and downhill slopes. J Appl Physiol 2002; 93:10391046.

    • Search Google Scholar
    • Export Citation
  • 10. Margaria R. Sulla fisiologia e specialmente sul consumo energetico della marcia e della corsa a varia velocità ed inclinazione del terreno. Atti Accad Naz Lincei 1938; 7:299368.

    • Search Google Scholar
    • Export Citation
  • 11. Woledge RC, Curtin NA, Homsher E. Energetic aspects of muscle contraction. London: Academic Press, 1985;268271.

  • 12. Higbie EJ, Cureton KJ, Warren GL, et al. Effects of concentric and eccentric training on muscle strength, cross-sectional area, and neural activation. J Appl Physiol 1996; 81:21732181.

    • Search Google Scholar
    • Export Citation
  • 13. Raab JL, Eng P, Waschler RA. Metabolic cost of grade running in dogs. J Appl Physiol 1976; 41:532535.

  • 14. Roig M, Macintyre DL, Eng JJ, et al. Preservation of eccentric strength in older adults: evidence, mechanisms and implications for training and rehabilitation. Exp Gerontol 2010; 45:400409.

    • Search Google Scholar
    • Export Citation
  • 15. Roig M, O'Brien K, Kirk G, et al. The effects of eccentric versus concentric resistance training on muscle strength and mass in healthy adults: a systematic review with meta-analysis. Br J Sports Med 2009; 43:556568.

    • Search Google Scholar
    • Export Citation
  • 16. Roig M, Shadgan B, Reid WD. Eccentric exercise in patients with chronic health conditions: a systematic review. Physiother Can 2008; 60:146160.

    • Search Google Scholar
    • Export Citation
  • 17. Seger JY, Arvidsson B, Thorstensson A. Specific effects of eccentric and concentric training on muscle strength and morphology in humans. Eur J Appl Physiol Occup Physiol 1998; 79:4957.

    • Search Google Scholar
    • Export Citation
  • 18. Seger JY, Thorstensson A. Effects of eccentric versus concentric training on thigh muscle strength and EMG. Int J Sports Med 2005; 26:4552.

    • Search Google Scholar
    • Export Citation
  • 19. Sexton WL, Erickson HH. Effects of treadmill elevation on heart rate, blood lactate concentration and packed cell volume during graded submaximal exercise in ponies. Equine Vet J Suppl 1990; 9:5760.

    • Search Google Scholar
    • Export Citation
  • 20. Zou K, Meador BM, Johnson B, et al. The α(7) β(1)-integrin increases muscle hypertrophy following multiple bouts of eccentric exercise. J Appl Physiol 2011; 111:11341141.

    • Search Google Scholar
    • Export Citation
  • 21. Paradisis GP, Bissas A, Cooke CB. Combined uphill and downhill sprint running training is more efficacious than horizontal. Int J Sports Physiol Perform 2009; 4:229243.

    • Search Google Scholar
    • Export Citation
  • 22. Taylor CR. Relating mechanics and energetics during exercise. Adv Vet Sci Comp Med 1994;38A:181215.

  • 23. Taylor CR, Caldwell SL, Rowntree VJ. Running up and down hills: some consequences of size. Science 1972; 178:10961097.

  • 24. Williams RJ, Nankervis KJ, Colborne GR, et al. Heart rate, net transport cost and stride characteristics of horses exercising at walk and trot on positive and negative gradients. Comp Exerc Physiol 2009; 6:113119.

    • Search Google Scholar
    • Export Citation
  • 25. Jones JH, Longworth KE, Lindholm A, et al. Oxygen transport during exercise in large mammals. I. Adaptive variation in oxygen demand. J Appl Physiol 1989; 67:862870.

    • Search Google Scholar
    • Export Citation
  • 26. Birks EK, Jones JH, Berry JD. Plasma lactate kinetics in exercising horses. In: Persson SGB, Lindholm A, Jeffcott LB, eds. Equine exercise physiology 3. Davis, Calif: ICEEP Publications, 1991;179187.

    • Search Google Scholar
    • Export Citation
  • 27. Fedak MA, Rome L, Seeherman HJ. One-step N2-dilution technique for calibrating open-circuit VO2 measuring systems. J Appl Physiol 1981; 51:772776.

    • Search Google Scholar
    • Export Citation
  • 28. Robert C, Valecte JP, Denoix JM. The effects of treadmill inclination and speed on the activity of two hindlimb muscles in the trotting horse. Equine Vet J 2000; 32:312317.

    • Search Google Scholar
    • Export Citation
  • 29. Bramble DM, Carrier DR. Running and breathing in mammals. Science 1983; 219:251256.

  • 30. Margaria R, Cerretelli P, Aghemo P, et al. Energy cost of running. J Appl Physiol 1963; 18:367370.

  • 31. Pivarnik JM, Sherman NW. Responses of aerobically fit men and women to uphill/downhill walking and slow jogging. Med Sci Sports Exerc 1990; 22:127130.

    • Search Google Scholar
    • Export Citation
  • 32. Minetti AE, Ardig OL, Reinach E, et al. The relationship between mechanical work and energy expenditure of locomotion in horses. J Exp Biol 1999; 202:23292338.

    • Search Google Scholar
    • Export Citation

Contributor Notes

Address correspondence to Dr. Jones (jhjones@ucdavis.edu).