J Comp Physiol B (2009) 179:839–845 DOI 10.1007/s00360-009-0367-z
ORIGINAL PAPER
Reliability of an incremental exercise test to evaluate acute blood lactate, heart rate and body temperature responses in Labrador retrievers Luca Ferasin · Samuele Marcora
Received: 2 January 2009 / Revised: 22 April 2009 / Accepted: 30 April 2009 / Published online: 20 May 2009 © Springer-Verlag 2009
Abstract Thirteen healthy Labrador retrievers underwent a 5-stage incremental treadmill exercise test to assess its reliability. Blood lactate (BL), heart rate (HR), and body temperature (BT) were measured at rest, after each stage of exercise, and after a 20-min recovery. Reproducibility was assessed by repeating the test after 7 days. Two-way MANOVAs revealed signiWcant diVerences between consecutive stages, and between values at rest and after recovery. There was also a signiWcant reduction in physiological strain between the Wrst and second trial (learning eVect). Test reliability expressed as typical error (BL = 0.22 mmol/l, HR = 9.81 bpm, BT = 0.22°C), coeYcient of variation (BL = 19.3%, HR = 7.9% and BT = 0.6%) and test–retest correlation (BL = 0.89, HR = 0.96, BT = 0.95) was good. Results support test reproducibility although the learning eVect needs to be controlled when investigating the exerciserelated problems commonly observed in this breed. Keywords collapse
Dogs · Canine · Treadmill · Exercise-induced
Communicated by G. Heldmaier. L. Ferasin College of Veterinary Medicine, University of Minnesota, St Paul, MN, USA S. Marcora School of Sport, Health and Exercise Sciences, Bangor University, Gwynedd, Wales, UK e-mail:
[email protected] L. Ferasin (&) 10 Brambridge House, Kiln Lane, Eastleigh, Hampshire SO50 6HL, UK e-mail:
[email protected]
Introduction Labrador retrievers represent the most common canine breed in the world (Wikipedia 2009). They are commonly used as pets, as well as working dogs in several activities, such as hunting, tracking/detection, disabled-assistance, and therapy work. Their ability to exercise is fundamental for successful performance of their tasks and exerciserelated problems can severely compromise the career of a dog even after a long and expensive period of training. Therefore, owners, trainers and veterinarians need objective parameters to assess the physical condition of these dogs. It is well known that exercise causes signiWcant acute responses in rectal temperature, pulse rate, blood lactate and other physiological parameters in healthy dogs (HinchcliV et al. 1993; Ilkiw et al. 1989; Matwichuk et al. 1999; Steiss et al. 2004). However, to the best of our knowledge, there are no available data that originate from standardized studies where test–retest reliability has been assessed. Furthermore, in the above-mentioned studies, most parameters were evaluated before and after intense exercise and did not evaluate the physiological responses that occur during exercise. Reproducible values originating from a validated test are necessary to meaningfully compare dogs and monitor the progress of individuals in response to training and clinical interventions (Ferasin and Marcora 2007). In fact, this knowledge can assist the investigator in discriminating genuine physiological changes that occur after treatment from within-subject inter-test variability. Similarly, the availability of a reliable test may be particularly useful to study the pathophysiology of exercise-related abnormalities in dogs, such as exercise intolerance and collapse. Although exercise tests in the Weld, such as during training or competitions, are easy to perform, a reproducible and
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standardized protocol can hardly be achieved. Conversely, the use of a motorized treadmill allows control of exercise intensity and duration, as well as environmental conditions, facilitating the standardization of the test. An online bibliographic search returned more than 600 citations on studies involving dogs exercising on a treadmill. However, most of the above studies involved experimental dogs chronically instrumented with invasive surgical techniques. The purpose of the present study was to assess the reproducibility of a non-invasive exercise test in healthy Labrador retrievers and evaluate blood lactate (BL), heart rate (HR) and body temperature (BT) responses that occur during and after incremental exercise in this breed.
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exhaustion. A 20-min recovery period was calculated from the end of the treadmill test or from the time of exhaustion. A 1-min pause between stages was necessary to collect blood samples and measure rectal temperature. A safety harness3 was attached to each dog to allow continuous control of the subject during exercise to prevent incidental falls and promptly remove weight bearing in a comfortable manner in case of exhaustion or sudden reluctance to move. During the test, all dogs wore dedicated canine boots4 to avoid foot injuries and increase the grip and traction on the treadmill. Owners were instructed not to feed their dogs during the 3 h preceding the test. However, dogs were allowed to drink fresh water before the test, during pauses and during the 20-min recovery period.
Methods and materials Measurement Animals Sixteen healthy client-owned Labrador retriever dogs (8 males and 8 females) participated in the present study. Written informed owner consent was obtained in each case. Study approval was granted by the Institutional Animal Care and Use Committee (IACUC) of the University of Minnesota.1 A full clinical history, including information on dietary regimens and average daily exercise was obtained from every dog’s owner. All dogs underwent a full physical examination to rule out possible clinical abnormalities that could aVect exercise performance, in particular cardio-vascular, neuromuscular and orthopedic conditions. All dogs’ details and body weights were recorded at the beginning of the study. Dogs were not pre-trained to run on a treadmill and were not familiar with the equipment. Exercise protocol Dogs underwent an exercise test on a motorized treadmill2 using a 6-min stage protocol at incremental speeds (6.0, 7.0, 8.0, 9.0, 10.0 mph) for a maximum of 30-min exercise. The slope was adjusted to 5 or 15% depending on the presumed Wtness of each individual dog based on the owner’s description of the type and duration of daily exercise assessed as part of a standardized medical questionnaire. Dogs were deemed to have reached exhaustion when they suddenly stopped running or lost coordination during exercise. When exhaustion was achieved before the end of the Wve stages, measurements were taken at the time of
1
Study protocol 0705A07843, approved on June 20 2007. L8 Rehabilitation Treadmill, Landice Inc., Randolph, New Jersey USA. 2
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Venous blood samples (approximately 50 l) were obtained by venipuncture from the jugular vein using a 25-gauge disposable needle directly mounted onto a syringe. Single measurements of lactate were made immediately after blood collection by an enzymatic-amperometric analyzer previously validated in dogs5 (Ferasin et al. 2007). Heart rate and electrocardiography (ECG) were monitored and recorded via radio-telemetry.6 Recording leads were connected to the dog’s thoracic wall via self-adhesive wet-gel electrodes7 and the radio-transmitter was Wxed to the dog’s harness. The attachment of ECG leads and radiotransmitter to the dog was carried out approximately 10 min before the beginning of the test. The continuous ECG recording was started at rest and stopped after the end of the recovery period and was monitored throughout the test to identify whether rhythm or conduction abnormalities developed during exercise. Thorough ECG analysis was carried out after completion of the trial. Heart rate was calculated by measuring and averaging Wve consecutive R-R intervals recorded before the beginning of the test (resting value), at the end of each stage, and after the 20-min recovery time [HR = 1,500/average RR (mm) at 25 mm/s recording)]. Rectal temperature was measured at rest, immediately after each exercise stage and at the end of the recovery period using a rapid reading digital thermometer.8
3
Web Master™, RuV Wear Inc., Bend, Oregon, USA. Bark'n Boots™ Grip Trex™, RuV Wear Inc., Bend, Oregon, USA. 5 Lactate Scout, Senslab, Leipzig, Germany. 6 Sapphire ECG, Vetronic, Newton Abbot, UK. 7 Blue sensor, M-00-S, Medicotest, Ølstykke, Denmark. 8 Mabis Healthcare, Waukegan, Illinois, USA. 4
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Equipment maintenance and laboratory environment
Results
The treadmill belt was cleaned, aligned and lubricated daily. The lactate monitor was calibrated on a daily basis before the beginning of the study using the manufacturer’s control solution. All instruments were operated in accordance with the manufacturer’s instructions. Laboratory environmental conditions were controlled by air conditioning and temperature and relative humidity were monitored and recorded at the beginning of each test. Dog owners were allowed to be present in the laboratory and verbally encourage their dogs during the test.
Three of the 16 dogs initially enrolled were removed from the study for the following reasons: one dog appeared particularly nervous and demonstrated reluctance to walk on the treadmill; another one showed signs of exhaustion just after the Wrst 5 min of exercise, while a third dog failed to represent for repeating the test the following week. All the remaining subjects (6 males and 7 females) successfully completed the trial. On the basis of the level of Wtness previously assessed by the dogs’ owners, 7 dogs (3 females and 4 males) were exercised with a 15% slope and 6 dogs (3 males and 3 females) with a 5% slope. Their mean age (§SD) was 3.6 (§1.6) years and their average body weight (§SD) was 29.4 (§5.3) kg. The mean (§SD) environmental temperature and humidity during the conduction of the trial was 23.5 (§0.4) °C and 28.8 (§2.4) percent, respectively. Four of the 13 subjects performed all Wve stages of the incremental test (30-min exercise), and appeared reluctant to undergo any further exertion. The remaining dogs reached exhaustion before completion of the Wnal stage. The mean (§SD) exercise time was 27 min and 21 s (§2 min and 19 s). In the second trial, none of the dogs achieved exhaustion before the end-point recorded in the Wrst part of the study. During recovery, all dogs adopted sternal or lateral recumbency and were heavily panting throughout the entire period. Moreover, most dogs appeared physically exhausted, showing pronounced muscular weakness aVecting, in particular, their hindlimbs and were unable to regain a natural standing position for several minutes. Nevertheless, they appeared comfortable, mentally bright and fully responsive and complete recovery was observed within a maximum of 20 min. Most owners reported to have observed similar features in their dogs after periods of short and intense exercise. The ECG recordings showed sinus rhythm throughout the test in all subjects. Premature complexes, conduction disturbances or rhythm abnormalities were never observed. Values of BL concentration, HR and BT measured at diVerent exercise levels followed a normal distribution in both trials. The test reliability is reported in Table 1 as TE, CV and TCC for the measurements of BL, HR and BT obtained in the two trials. The lower and upper 95% limits of agreement are also indicated. Results obtained from measurements of BL and HR showed heteroscedasticity and data were log-transformed prior to calculation. Mean responses (§SEM) of BL, HR and BT obtained in the two trials during the incremental treadmill test and after recovery time are shown in Fig. 1. Fully-repeated two-way MANOVA showed that all the within-subject measurements were signiWcantly diVerent both between stages and between trials, without signiWcant interaction, as indicated in Fig. 1. Results of Bonferroni follow-up tests of the main eVect of
Test reproducibility The exercise study was repeated 7 days after completion of the Wrst test, at the same time of the day and under the same environmental conditions. In the second trial, the test endpoint for each individual was set at the same time of exhaustion recorded in the Wrst trial. Vigorous exercise of the subjects in the 12 h preceding the test and changes in the level of exercise and diet between the Wrst and the second trial were discouraged. Statistical analysis Data distribution of BL, HR and BT values measured at rest, at the end of each exercise stage and at the end of the recovery period were assessed for normality using the D’Agostino–Pearson test. The test reliability/reproducibility was assessed by calculating the typical error (TE) (standard deviation in each subject’s measurements between tests; TE = SD(diV)/q2), coeYcient of variation (CV) [within-subject variation expressed as a percent of the subject’s mean; CV = 100(eSD/100 ¡ 1)] and test–retest correlation coeYcient (TCC) (Pearson correlation coeYcient between the two trials), as described by Hopkins (2000). Data showing heteroscedasticity were log-transformed before calculations. A fully-repeated two-way multivariate analysis of variance (MANOVA) was performed to evaluate the withinsubject eVect of exercise stage and trial repetition. Where statistical signiWcance (P < 0.05) for main-eVect stage was observed, a paired t test with Bonferroni correction was used to establish statistical diVerences between values obtained during consecutive stages. Statistical calculations were performed using SPSS statistics software9 and Microsoft OYce Excel.10
9
SPSS 16.0 Software, Chicago, Illinois, USA. Microsoft OYce Excel XP 2003, Microsoft Corporation, US.
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Table 1 Typical error (TE), coeYcient of variation (CV) and test– retest correlation coeYcient (TCC) of blood lactate, heart rate and body temperature measured in the two consecutive trials
Table 2 Post hoc tests of the main eVect of stage on blood lactate, heart rate and body temperature using paired t tests with Bonferroni correction
Parameter
Comparison
Blood lactate
Heart rate
Temperature
TE
CV
Blood lactate
0.22 (0.19; 0.27)
19.3 (16.3; 23.8) 0.89 (0.83; 0.93)
Heart rate
9.81 (8.39; 11.83) 7.9 (6.7; 9.5)
Body 0.22 (0.19; 0.26) temperature
0.6 (0.5; 0.7)
TCC
Resting–Stage 1
0.029584
0.000000*
0.000001*
0.96 (0.93; 0.97)
Stage 1–Stage 2
0.002361*
0.046798
0.000020*
0.95 (0.93; 0.97)
Stage 2–Stage 3
0.000310*
0.082874
0.000001*
Stage 3–Stage 4
0.025292
0.924003
0.000000*
Stage 4–Stage 5
0.001095*
0.843351
0.000151*
Stage 5–recovery
0.275081
0.000000*
0.000000*
Recovery–resting
0.000002*
0.000035*
0.000000*
TE units for blood lactate, heart rate and body temperature are displayed in mmol/l, beats per minute (bpm) and Celsius (°C), respectively. CV is expressed in percent (%). TCC is illustrated as Pearson’s correlation coeYcient (r). Values in brackets represent the lower and upper 95% conWdence limits
* P < 0.007 according to Bonferroni correction: 0.05/7
stage are reported in Table 2, showing the statistical diVerences between consecutive stages and between resting values and values recorded after recovery. In none of the 13 subjects examined in this study could an abrupt increase in BL concentration be detected, indicating that a lactate threshold during this type of exercise is not demonstrable in Labrador retrievers
Fig. 1 Mean variations (§SEM) of blood lactate (a), heart rate (b) and body temperature (c) obtained in the two trials during the incremental treadmill test and after recovery time. The (n) value indicates the number of dogs that completed the entire 6-min stage. Results (F and
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Discussion One of the major limitations in companion canine exercise testing described in the literature is the apparent unwillingness of dogs to walk or run on a motorized treadmill without
P value) of the fully-repeated two-way multivariate analysis of variance (MANOVA) are indicated as “” (within-subject eVect of exercise stage) and “” (within-subject eVect trial repetition)
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previous training (Kittleson et al. 1996) although in our own previous studies we did not identify such diYculties in untrained dogs (Ferasin et al. 2005; Ferasin and Marcora 2007). In our previous studies, dogs were led by their owners on a suYciently wide treadmill and the presence of the owner was probably suYcient to reduce the dogs’ anxiety. In the present study, which involved much faster speeds, dogs run alone on the treadmill but were secured with a comfortable safety harness held by an operator standing above them. In addition, their owners were present in the room and were allowed to incite and encourage their dogs during the trial. We believe that these laboratory conditions contributed to reassure these dogs to run fearlessly on the treadmill. Furthermore, dogs appeared very keen to repeat the test 1 week later. The results of the present study conWrm again that even dogs that are unfamiliar to the laboratory environment and have never exercised on a treadmill can usually undergo incremental exercise testing successfully. However, in this study it was noticed that dogs become acquainted with the test and learned how to run more eYciently on the treadmill on the second trial, thereby reducing their physiological strain. Indeed, one of the most important pieces of information that emerges from this study is a modest, yet statistically signiWcant, diVerence between trials. All recorded values (BL, HR and BT) were signiWcantly lower in the second trial, which suggests a reduction in physiologic stress when the test is repeated in dogs unfamiliar with treadmill exercise. A signiWcant decrease in HR may be caused by a reduction in anxiety. However, concomitant changes in BL and BT suggest that these dogs learned to run on a treadmill more eYciently. This learning eVect needs to be considered when designing experimental studies where either a randomized control group or counterbalanced assignment of treatment needs to be implemented. Another strategy which may also be useful when monitoring longitudinal changes in individual dogs due to development/ageing or treatment (physical training, medications, diet, etc.) is to add a familiarization session before baseline testing. Further reliability studies in which subjects are tested three or more times are needed to assess the usefulness of such strategy in dogs. In spite of the learning eVect discussed above, all other measures of reliability show good reproducibility (Hopkins 2000) The greatest variability between the two trials was observed in BL concentrations, with a CV of nearly 20%. It should be noticed, however, that this CV is lower than in exercising humans (Saunders et al. 2004), and that the TCC of BL was relatively high (r = 0.89) and the typical error was only 0.22 mmol/l, which approaches the analytical variability of the instrument used in the study (Ferasin et al. 2007). All measures of reliability showed good reproducibility for both HR and BT. It is also quite conceivable to
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believe that between trials variability of all physiological responses might have been even lower if dogs were familiar with treadmill exercise, as previously observed in humans (McGawley and Bishop 2006). In contrast with what has been observed in people (McArdle et al. 2000; Svedahl and MacIntosh 2003; Tokmakidis et al. 1998), incremental exercise did not appear to induce abrupt increases in BL concentration in Labrador retrievers, although signiWcant variation was observed between stages. Moreover, in humans, BL concentrations would be expected to decrease during recovery after intense exercise (Dodd et al. 1984; Stamford et al. 1978). However, BL values remained stable after a 20-min recovery in all dogs used in this study. Blood lactate concentration during exercise is the result of lactate production by the contracting muscle, lactate transport from the muscle to the vascular bed, as well as intracellular and hepatic clearance (Gladden 2004; Messonnier et al. 2006). Assuming that lactate clearance would not cease during recovery and that lactate production in the muscle would not continue after termination of the exercise, it can be speculated that the modest increase of lactate values observed in Labradors depends on a slow transport of this compound from muscle to blood. This could be caused by a low muscular density of proteins involved in lactate transport (i.e., monocarboxylate transporter) and/or intracellular lactate clearance (Messonnier et al. 2007). However, further studies are necessary to establish whether the lactate dynamics observed in these dogs during incremental exercise are truly due to a slow lactate clearance induced by either of these mechanisms. The modest changes in BL during exercise did not allow an easy identiWcation of individual lactate thresholds described in humans, either as abrupt sustained increase in BL (Davis et al. 1976) or Wxed concentration at 2 or 4 mmol/l (Sjodin and Jacobs 1981). However, by adopting the system proposed by Yoshida et al. (1987) where lactate threshold is deWned as a 1 mmol/l increase above the resting value, identiWcation of lactate threshold was possible in 5 of the 13 dogs. Heart rate increased signiWcantly after the Wrst exercise stage but further signiWcant increments were not observed during the following stages. This is in contrast with the linear increase in HR observed in humans (McArdle et al. 2000) and in chronically instrumented dogs (Ordway et al. 1984) during incremental exercise. Considering that cardiac output is expected to increase during incremental exercise, a signiWcant change in stroke volume, rather than heart rate, would be expected in these dogs. Stroke volume can increase during exercise due to enhanced cardiac contractility, reduced systemic vascular resistance and increased central venous pressure (Levick 2003), and deserves further investigations. In our study, it was also observed that HR increased at the beginning of each stage and then reached a lower and
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stable value after only a few minutes. Mean HR declined signiWcantly after the recovery period, approaching the resting value recorded before the test. Heart rate responses during exercise are primarily controlled by the autonomous nervous system and represent important parameters for clinical applications (Arai et al. 1989; Pierpont et al. 2000) As observed in humans (McArdle et al. 2000), body temperature increased progressively during exercise and decreased after the recovery period. Mean BL, HR and BT values post-recovery were still signiWcantly higher than resting values, suggesting that a longer resting period is necessary to restore all baseline parameters after this test. Furthermore, BL kinetics might have been aVected by intermittent exercise, due to the technical pauses between stages (Tokmakidis et al. 1998). The prolonged recumbency and the temporary inability to regain the quadrupedal posture observed in most dogs during the recovery time resemble the features of exerciseinduced collapse observed in some Labrador retrievers after intense exercise (Taylor et al. 2008). This exertional fatigue could be attributed to a variety of reasons. Exercise-induced changes in muscle action potential, extracellular and intracellular ions, and intracellular metabolites reduce the ability to produce force (peripheral fatigue) (Allen et al. 2008). Changes at spinal and supraspinal level due to alterations in brain metabolism and neurotransmitters, or inhibitory aVerent feedback from type III and IV muscle aVerents can also reduce the ability of the CNS to activate the locomotor muscles (central fatigue) (Gandevia 2001). It is also possible that, in these dogs, the increased pulmonary blood Xow and capillary pressure during intense exercise induced the activation of pulmonary C Wbers (or J receptors). This activation can evoke a somatomotor reXex (the J reXex) that provides potent inhibition of limb muscles in animals but not humans (Gandevia et al. 2000). The incremental exercise test in Labrador retrievers described in this study could represent a suitable animal model to study the role played by the J reXex in causing exercise intolerance and collapse in Labrador retrievers and, possibly, other canine breeds. In conclusion, the incremental exercise test described in this study appears feasible and provides reproducible information on the acute BL, HR and BT responses to exercise in Labrador retrievers. However, some limitations need to be addressed. First, it is clear that these dogs learn how to run more eYciently and less fearfully on the treadmill on the second trial, thereby reducing physiologic stress. This phenomenon needs to be considered when designing and evaluating experimental exercise studies, and may be eliminated by performing a familiarization trial before baseline testing. A familiarization trial may also improve test–retest reproducibility by reducing the variability associated with the learning eVect. Finally, a familiarization trial might be useful to provide more objective information on the level of
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Wtness of single individuals, rather than relying solely on the subjective assessment of their owners. Further studies are necessary to conWrm these hypotheses and to investigate in more detail the peculiar physiological responses to exercise observed in the dogs in this study. This test may also be useful to investigate mechanisms of exhaustion and the cause of prolonged recumbency or collapse (exerciseinduced collapse) frequently observed following intense exercise in Labrador retrievers (Taylor et al. 2008). Acknowledgments We would like to thank all the owners of the dogs involved in this study for their precious support and encouragement. A special thank you to Heidi Cooper, Jaime Shriver and Christopher McKinney for their invaluable technical assistance. Some of the results of the present study have been presented at the ECVIM-CA annual congress, Ghent, Belgium, 4–8 September 2008. This study was supported by the Department of Clinical Veterinary Sciences, University of Minnesota, USA.
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