SEARCH

SEARCH BY CITATION

Keywords:

  • horse;
  • HPA;
  • showjumping;
  • training;
  • total and free iodothyronines

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion and conclusions
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

Reasons for performing study: Limited knowledge exists about the differentiated effects of competitive and noncompetitive showjumping on thyroid function and relationships with hypothalamic-hypophysis-corticoadrenal hormones.

Objectives: To obtain preliminary data about differentiated effects of competitive and noncompetitive showjumping on total and free iodothyronines, β-endorphin, ACTH and cortisol of horses.

Material and methods: Five trained healthy jumper horses were studied during competitive and noncompetitive showjumping, performed in the same circuit design over 10 fences of 1.10 m. Hormone levels before, 5 and 30 min post exercise were recorded. Serum iodothyronines and cortisol concentrations were measured in duplicate utilising EIA kits. Serum ACTH and plasma β-endorphin concentrations were analysed in duplicate utilising RIA kits. Two-way RM ANOVA was applied to test for effects of interaction between different type of session and time. Significant differences between post exercise and basal values were established using Bonferroni's multiple comparison test. A linear correlation analysis (Pearson's method) was performed to analyse the relationships between total and free iodothyronines and between iodothyronines and β-endorphin, ACTH and cortisol.

Results: In sampling times adopted no statistical different effects of type of session were recorded on hormone variables. Sampling time affected ACTH (F = 4.25; P<0.02) and T4 (F = 4.43; P<0.02) post exercise changes. During the noncompetitive session, significant correlations existed between T4 and β-endorphin (r =−0.56), ACTH (r =−0.65), between β-endorphin and ACTH (r = 0.52) and between T3 and fT3 (r = 0.72); during competition between β-endorphin and T3 (r =−0.67), fT3 (r =−0.59).

Conclusions: These preliminary results could demonstrate correlations between thyroid hormones and β-endorphin response to showjumping, although no definitive conclusion can be produced concerning the relationships between HPA and thyroid function during exercise.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion and conclusions
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

In different species, previous studies have shown that deleterious effects of stress are only observed in animals submitted to a physical stressor associated to psychological factors (Maier 1993).

It is well known that the hypothalamic-pituitary-adrenal (HPA) axis plays a role in the coping response to metabolic and stressful challenges during exercise and secretion of β-endorphin, ACTH and cortisol is modulated by type, intensity and duration of exercise (Lekeux et al. 1991; McCarthy et al. 1991; Art et al. 1994; Rose and Hudgson, 1994; Foreman and Ferlazzo 1996; Ferlazzo and Fazio 1997; Kurosawa et al. 1998; Mehl et al. 1999, 2000; Nagata et al. 1999; Ferlazzo et al. 2007). It has been also reported that novelty stimuli during an exercise test increases plasma ACTH (Hada et al. 2003) and that emotional stress prior to a competition (Ferlazzo et al. 1993) as well as the level of competition experience (Cayado et al. 2006) affects ACTH and cortisol responses and these results suggest that horses become conditioned to the psychological stress of the show environment (Clayton 1989). Moreover, there are actual limited data concerning the effects of exercise on β-endorphin in horses during competition stress with respect to training (Cayado et al. 2006; Ferlazzo et al. 2009).

The effects of exercise on circulating iodothyronines remain controversial and little is known about the relationships between HPA and HPT axis in horses. In different species, peripheral T3 levels were related to psychological coping of stress response (Helmreich et al. 2006).

Thyroid hormones are usually involved in the control of metabolic rate and animal thermogenesis and are also related to central nervous system development and cognitive function and have been previously linked to exercise adaptation in different species (Sander and Rocker 1988; Panciera et al. 2003) and equine performance (Thornton 1985; Ferlazzo and Fazio 1997; Ferlazzo et al. 2007) and are mainly affected by the severity of exercise. In human subjects, moderate and high intensity of exercise caused TSH increases (Surks et al. 2005; Ciloglu et al. 2006) which appeared within minutes, while intermediate and long-term response to exercise remains unclear (Brabant et al. 2005)

Therefore, it would be worthwhile investigating whether psycho-physical stressors associated to showjumping could influence the HPA axis and thyroid function and whether a relationship exists between these neuroendocrine systems in horses.

The aim of this study was to obtain preliminary data on the hormonal response (β-endorphin, ACTH, cortisol, total and free iodothyronines) of horses submitted both to competitive and noncompetitive showjumping in order to compare the differentiated effects of exercise on thyroid function and its relationship with HPA hormones.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion and conclusions
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

Horses

All methods and procedures used in this experiment were reviewed and approved by the Messina University Institutional Board for the Care and Use of Animals.

Five trained sport jumper horses (4 Sella Italiano and 1 Dutch Warmblood), 3 geldings and 2 mares, aged 6–12 years (average 6.6 years) and weight 575 ± 52 kg were used. The study was carried out at the Equine Research Facility where all horses were housed in individual boxes of 4 × 4 m. Each horse was fed twice a day with 3–4 kg/day of a commercially available hay cube ration and approximately 7 kg/day of alfalfa and grass hay. Water and a salt/mineral block were ad libitum available for the horses all times. All horses were in regular training for 2–3 years, usually 1 h once daily, approximately 4–5 days/week with the same rider for each horse. The horses were able to cope with fences up to 1.30 m high and they all had previous experience of showjumping competition. At time of blood sampling, all horses were under regular training and considered by the referring veterinarian as clinically healthy.

Each horse was exercised once daily over 4 consecutive days prior to the sessions for 10 min warm-up at walk, trot and quiet canter and they also jumped 3 low fences.

All horses were studied during 2 different exercise conditions. The horses were subjected to a noncompetitive showjumping session (Session A). Then, after one week, the same horses participated in a competitive showjumping event (Session B). Both sessions were carried out in an outdoor arena (33.77 m wide × 70.33 m long) and performed the same circuit design over 10 fences of 110 cm, with 5 upright and 5 cross-pole fences.

The weather was sunny, with an outdoor mean temperature of approximately 13–14°C. The horses performed the 2 sessions with the same rider.

Heart rate was monitored with a Polar Sport Tester1, which recorded heart rate at 15 s intervals. One electrode was placed under the girth behind the left elbow, the other under the saddle at the withers. Heart rate was recorded at 15 intervals during the courses and until 30 min after completing the courses. Heart rate was adopted as a quantitative measure to assess workloads of different showjumping sessions.

The competitive and noncompetitive sessions were cantered at an average speed of approximately 350 m/min and were scored by time and knockdowns on the courses. Time for completion of the courses and therefore the speed of each course were registered. Fault and refusal of each horse were also registered.

Blood sampling and hormone analysis

Blood samples (10 ml) were collected from the jugular vein using evacuated tubes2, at 3 time points: baseline at rest (between 07.00 and 08.00 h), then 5 and 30 min after both sessions. On the day of blood sampling no restraint was necessary as the horses were familiar with handling procedures. Informed consent from horse owners was provided.

Blood samples were centrifuged at 3000 g for 15 min and the obtained sera samples stored at −20°C until analysed.

In order to analyse β-endorphin concentrations, an aliquot of the blood samples (2.5 ml) was transferred after collection into polypropylene tubes containing EDTA (1 mg/ml of blood) and aprotinin3 (500 Kallikrein Inhibitor Unit/ml blood), and kept at 4°C. Plasma samples were separated and stored at −80°C until analysed. Peptides were extracted from plasma samples with 1% trifluoroacetic acid (TFA, HPLC grade) and elution with 60% acetonitrile (HPLC grade) in 1% TFA. Plasma β-endorphin concentrations were measured in duplicate utilising a commercial RIA kit4 for human β-endorphin, which has a 100% cross-reactivity with equine β-endorphin (Mehl et al. 1999, 2000). The hormone assay utilised has a range for the amount of β-endorphin detected of 1–128 pg/100 µl (3–371 pmol/l). The respective inter- and intra-assay CVs were 7 and 15%.

Serum ACTH concentrations were analysed in duplicate using a commercially available radioimmunoassay kit5 (ELSA-ACTH) suitable for equine use (Ferlazzo et al. 1998). The hormone assay utilised had an ACTH detection range of 0-440 pmol/l. Intra- and inter-assay CV were 6 and 15%, respectively.

Total serum cortisol concentrations were analysed in duplicate using a commercial competitive enzyme assay6. The assay sensitivity was 5 ng/ml. The intra- and inter-assay CVs were 4 and 6.9%, respectively.

Serum total and free iodothyronines (T3, T4, fT3, fT4) concentrations were analysed in duplicate using a commercial ES300 Testing Procedure based on a commercial ELISA/competition to polyclonal biotinylated ovine iodothyronine-antibodies using streptavidin technology7 suitable for equine use (Ferlazzo et al. 1996). The respective intra- and inter-assay CVs were as follows: 11.4 and 7.3% for T3, 5.7 and 2.3% for T4, 11.9 and 4.2% for fT3, 9.6 and 6.6% for fT4.

Statistics

Data are expressed as mean ± s.d. Results were analysed using statistical analysis software8. A 2-way analysis of variance with repeated measures (2-way RM ANOVA) was applied to test for the effects of different type of session and sampling times, as well as for the interaction between them, on hormonal concentrations. When the F statistic was significant, the differences between individual means over time were then assessed using a post hoc multiple comparison test (Bonferroni). A linear correlation analysis (Pearson's method) was performed to analyse the relationships between total and free iodothyronines and between iodothyronines and β-endorphin, ACTH and cortisol. Statistical significance was set at P<0.05.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion and conclusions
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

Result of performance

The horses showed different performances with no refusals. Session A: clear round: n = 5; Session B: clear round: n = 4; penalty round: n = 1.

Speed

The mean speed during both exercises was 5.6 ± 0.4 m/s and mean duration 86.3 ± 1.5 s.

Heart rate

The horses had a mean heart rate of 95.7 ± 4.3 beats/min at the end of 10 min warm-up, which decreased to a mean of 45.6 ± 2.7 beats/min in average 15 min. Heart rate increased from a mean of 42.3 ± 4.2 beats/min at the start of both sessions to a mean of 184.5 ± 2.1 beats/min at the end of the courses. The mean peak heart rates during Session A and Session B were, respectively, 183.5 ± 7.1 and 185.4 ± 8.2 beats/min. During recovery, heart rate decreased to a mean of 72.3 ± 8.8 beats/min after 5 min and was <50 beats/min after 30 min.

β-endorphin

In Session A, β-endorphin concentrations showed (Table 1) a trend to be higher than basal 5 min post exercise, declining after 30 min. In Session B, increased β-endorphin concentrations were recorded after 30 min. The interaction type of session/sampling time was not significant.

Table 1. Circulating levels of β-endorphin, ACTH, cortisol and total and free iodothyronines in jumping horses during noncompetitive (Session A) and competitive (Session B) sessions
 Session ASession B
Basal5 min30 minBasal5 min30 min
β-endorphin (pmol/l)36.8 ± 19.1750.8. ± 14.0940.4 ± 7.4444.4 ± 13.2444.6 ± 17.9256.4 ± 25.27
ACTH (pmol/l)2.36 ± 0.703.68 ± 2.032.23 ± 1.021.88 ± 0.334.24 ± 2.372.88 ± 1.34
Cortisol (nmol/l)112.16 ± 53.58160.84 ± 21.65140.28 ± 19.0199.66 ± 15.78128.06 ± 64.54127.58 ± 27.27
T3 (nmol/l)0.73 ± 0.250.99 ± 0.371.02 ± 0.171.11 ± 0.311.00 ± 0.580.96 ± 0.38
T4 (nmol/l)31.24 ± 8.8731.76 ± 8.8243.86 ± 8.6729.39 ± 7.1641.08 ± 11.5743.78 ± 14.22
fT3 (pmol/l)2.55 ± 0.893.11 ± 1.072.84 ± 0.512.72 ± 1.443.53 ± 1.973.57 ± 1.98
fT4 (pmol/l)7.79 ± 3.477.80 ± 3.1110.80 ± 3.879.71 ± 2.518.36 ± 4.1716.03 ± 10.8

Adrenocorticotropin

With respect to basal values, ACTH concentrations showed (Table 1) a trend to increased levels 5 min post exercise and declined after 30 min both in Session A and in Session B, with values still higher in Session B than in Session A. The interaction type of session/sampling time was not statistical significant. Sampling time significantly affected post exercise ACTH changes (F = 4.25; P<0.02).

Cortisol

With respect to basal values, cortisol concentrations showed (Table 1) a trend to increased levels 5 min post exercise, declining after 30 min in Session A, while in Session B increased comparable concentrations were recorded both at 5 and 30 min post exercise. The interaction type of session/sampling time was not significant.

Serum total and free iodothyronines

In Session A, slightly higher than basal post exercise T3 values were recorded both at 5 and 30 min. After Session B, T3 showed lower than basal values at 5 and 30 min (Table 1).

In Session A, T4 concentrations were slightly modified post exercise, while increased 30 min post exercise. After Session B, slightly higher than basal values were recorded both 5 and 30 min post exercise (Table 1).

After Session A, fT3 showed slightly higher than basal values at 5 min, declining after 30 min. After Session B, fT3 showed higher than basal concentrations both at 5 and 30 min (Table 1).

In Session A, fT4 concentrations were slightly modified post exercise and were increasing after 30 min. In Session B, fT4 showed lower than basal values 5 min post exercise with a further increase at 30 min (Table 1).

The interaction type of session/sampling time was not significant for all variables. Sampling time significantly affected post exercise T4 changes (F = 4.43; P<0.02).

Correlation analyses

In Session A (Fig 1) positive correlation was found between β-endorphin and ACTH changes (r = 0.52; P<0.04). Moreover, T4 levels showed negative correlation with β-endorphin (r =−0.56; P<0.03) and ACTH changes (r =−0.65; P<0.009). Positive correlation was found between T3 and fT3 changes (r = 0.72; P<0.002).

image

Figure 1. Correlation analysis was performed on all data points of T4and β-endorphin (a), T4and ACTH (b) levels in 5 jumping horses during not competitive session. Coefficients of correlation (r), coefficients of determination (r2) and P values are indicated.

Download figure to PowerPoint

In Session B (Fig 2), negative correlations were found between β-endorphin and T3 changes (r =−0.67; P<0.006) and between β-endorphin and fT3 changes (r =−0.59; P<0.01).

image

Figure 2. Correlation analysis was performed on all data points of T3and β-endorphin (a), fT3and β-endorphin (b) levels in 5 jumping horses during competitive session. Coefficients of correlation (r), coefficients of determination (r2) and P values are indicated.

Download figure to PowerPoint

Discussion and conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion and conclusions
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

The hormone mean basal values were consistent with resting minimum values of β-endorphin (Hydbring et al. 1996; Ferlazzo et al. 1998; Mehl et al. 1999; Fazio et al. 2000) and ACTH (Cayado et al. 2006), reported for horses, including jumpers. Basal values were in the range reported for horses for cortisol (James et al. 1970; Hoffsis et al. 1979; Irvine and Alexander 1994) and total and free iodothyronines (Anderson et al. 1988; Bayly et al. 1996; Ferlazzo et al. 1996; Breuhaus et al. 2006).

The results of this study demonstrated that showjumping in trained horses did not induce significant post exercise increases in HPA and thyroid hormone concentrations or any statistically significant difference between competitive and noncompetitive sessions. This could be dependent on the training status of horses studied and to short term, low intensity and speed of showjumping exercise, which was certainly below the critical threshold for β-endorphin (Mehl et al. 2000) and ACTH (Nagata et al. 1999) secretion. However, this hypothesis cannot be confirmed because of lack of lactate evaluation.

The noncompetitive session induced parallel β-endorphin and ACTH modifications which increased 5 min post exercise as well as parallel modifications on the decrease afterwards, inducing significant positive correlation. This is in agreement with previous studies in man and horses (Goldfarb et al. 1987; McCarthy et al. 1991).

In competitive showjumping, basal β-endorphin concentrations were higher than in noncompetitive sessions and exercise induced a trend to increased levels exclusively at 30 min. Therefore, during competition a pre-exercise β-endorphin increase could be necessary for a tighter control of physical and emotional stress and it is likely that changes were dependent on exercise as well as on the emotional component of competition stress individually experienced by horses. Submaximal levels of treadmill exercise produced significantly increased β-endorphin concentrations, but differential responses between fit and unfit horses (McCarthy et al. 1991); training enhanced its response to acute exercise and time of peak concentration differed according to age of horses (Malinowski et al. 2002).

ACTH values tended to increase 5 min post exercise, declining afterwards. It is not clear whether the poor ACTH response to showjumping would represent the effect of a major increase induced in precompetition by emotional stress (Hada et al. 2003) variously suffered by the horses, or the actual absence of significant effects as a consequence of low intensity exercise (Nagata et al. 1999). The failure to demonstrate significant differences in β-endorphin as well as in ACTH levels post competition and of significant correlation could be explained by the high individual variability of values, probably explained by the different horses temperament and consequent individual catecholamine secretion (Snow et al. 1992).

The results demonstrated a trend to moderate cortisol increase 5 min post exercise during both sessions, with a tendency to remain elevated exclusively post competition. The results are consistent with data reported as an effect of different type of exercise, such as showjumping (Lekeux et al. 1991; Linden et al. 1991; Ferlazzo and Fazio 1997; Ferlazzo et al. 2007). However, the training status of horses being adapted to showjumping events of the same level could explain the lack of significant effects.

T3 concentrations tended to an increase after the noncompetitive session and decreased 5 and 30 min post competition, as reported in horses after endurance exercise, which showed greater decreases over longer distances (Graves et al. 2006). Showjumping probably induced an extrathyroidal supply of T3, as a consequence of the improved circulation (Art et al. 1994) and increase of 5-desiodase activity in muscle, for increased tissue hormone utilisation, as well as in other tissues participating to exercise stress coping, like brain (Rudas et al. 2005), where degrees of arousal in man are known to covary with iodothyronine levels (Tucker et al. 1984); the post competition T3 decrease could demonstrate such an increased tissue T3 utilisation, as shown in man and canine endurance athletes (Rone et al. 1992; Panciera et al. 2003).

A trend to moderate T4 and fT4 increases was recorded 30 min in post competitive and noncompetitive sessions, while fT3 values tended to increase 5 min post exercise, with higher levels in competitive than noncompetitive sessions at 30 min. Exercise-induced changes in serum iodothyronines concentrations have been previously reported in horses as well as in man and dogs (Irvine 1967, Terjung and Winder 1975; Garcia and Beech 1986; Ferlazzo and Fazio 1997; Panciera et al. 2003; Ferlazzo et al. 2007) and previous work has found considerable variability in iodothyronine response to acute short term and more prolonged exercise. The most physiological relevant factors that influence circulating thyroid hormone concentrations with exercise appear to be frequency and intensity of exercise and total amount of work performed. Previous studies showed T4 and fT4 levels significantly modified 24 h post showjumping competition (Fazio et al. 1994). Short term high intensity exercise during competition induced increments in T4 and T3 levels, with parallel changes to plasma catecholamines and a decrease in β-AR concentration of the erythrocyte membrane (Gonzáles et al. 1998). Significant increments in T4 plasma concentrations was found in man both after aerobic and anaerobic exercise, whilst T3 increased transiently only after aerobic exercise (Hackney and Gulledge 1994). Nevertheless, statistical analysis of data showed that the time of blood sampling significantly affected T4 post exercise changes and thus could have influenced the pattern of iodothyronine changes after showjumping. Therefore, frequency and duration of blood sampling represent a limit to correctly understanding these data.

Concerning the relationships between iodothyronines and HPA hormones, T4 levels were negatively correlated with β-endorphin and ACTH changes in a noncompetitive session, while in competition negative correlations were found between β-endorphin and T3 as well as between β-endorphin and fT3 changes. Various studies have already reported interactions between thyroid and adrenocortical function in man (Sanchez-Franco et al. 1989; Lo et al. 1998) and these results suggest a possible role of hypophyseal hormones in controlling thyroid secretion in the recovery phase.

No definite conclusions can be made from these preliminary results leading to the question of the physiological relevance concerning the association of HPA hormones and thyroid function during physical and emotional exercise stress during showjumping. Nevertheless, these data suggest the opportunity to carry out further investigations, supported by more essential control studies.

Manufacturers' addresses

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion and conclusions
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References

1 Polar Electro Europe BV, Fleurier, Switzerland.

2 Terumo®, Leuven, Belgium.

3 ICN Biomedicals Inc., Aurora, Ohio, USA.

4 Peninsula Laboratories Inc., Belmont, California, USA.

5 CIS-BioInternational, Gif-sur-Yvette, France.

6 RADIM/SEAC Co., Florence, Rome, Italy.

7 Roche Diagnostics GmbH, Mannheim, Germany.

8 SAS/STAT, Version 8.0; SAS Institute Inc., Cary, North Carolina, USA.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion and conclusions
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References
  • Anderson, R.R., Nixon, D.A. and Akasha, M.A. (1988) Total and free thyroxine and triiodothyronine in blood serum of mammals. Comp. Biochem. Physiol. 89A, 401-404.
  • Art, T., Franchimont, P. and Lekeux, P. (1994) Plasma β-endorphin response in thoroughbred horses to maximal exercise. Vet. Rec. 135, 499-503.
  • Bayly, W., Andrea, R., Smith, B., Stenslie, J. and Bergsma, G. (1996) Thyroid hormone concentrations in racing Thoroughbreds. Pferdeheilkunde 12, 534-538.
  • Brabant, G., Schwieger, S., Knoweller, R. and Tegtbur, U. (2005) Hypothalamic-pituitary-thyroid axis in moderate and intense exercise. Horm. Metab. Res. 37, 559-562.
  • Breuhaus, B.A., Refsal, K.R. and Beyerlein, S.L. (2006) Measurement of free thyroxine concentration in horses by equilibrium dialysis. J. vet. intern. Med. 20, 371-376.
  • Cayado, P., Muñoz-Escassi, B., Domínguez, C., Manley, W., Olabarri, B., Sánchez de la Muela, M., Castejon, F., Marañon, G. and Vara, E. (2006) Hormone response to training and competition in athletic horses. Equine vet. J., Suppl. 36, 274-278.
  • Ciloglu, F., Peker, I., Pehlivan, A., Karacabev, K., Ilhan, N., Saygin, O. and Ozmerdivenli, R. (2006) Exercise and intensity and its effects on thyroid hormones. Neuro Endocrinol. Lett. 26, 830-834.
  • Clayton, H.M. (1989) Terminology for the description of equine jumping kinematics. J. equine vet. Sci. 9, 341-348.
  • Fazio, E., Alberghina, D., Aronica, V., Medica, P. and Ferlazzo, A. (2000) Effect of performance success on blood β-endorphin, ACTH and cortisol levels in showjumping horses. In: The Elite ShowJumper, Ed: A.Lindner, Science Consult, Essen, Germany. pp 113-115.
  • Fazio, E., Murania, C., Medica, P. and Ferlazzo, A. (1994) Iodotironine totali e libere del siero nel Cavallo dopo attività fisica di tipo competitivo. Atti Soc. it. Sci. vet. 48, 125-129.
  • Ferlazzo, A. and Fazio, E. (1997) Endocrinological variables in blood and plasma. In: Performance Diagnosis of Horses, Ed: A.Lindner, Wageningen Press, Wageningen. pp 30-43.
  • Ferlazzo, A., Fazio, E., Aronica, V., Di Majo, R., Medica, P. and Grasso, L. (1998) Circulating concentrations of β-endorphin, ACTH and cortisol in horses after jumping over fences of different size. In: Proceedings of the Conference on Equine Sports Medicine and Science (Córdoba, Spain) pp 53-56.
  • Ferlazzo, A., Fazio, E., Iannelli, N., Murania, C., Panzera, M. and Piccione, G. (1993) Cortisolemia nel Cavallo atleta in corso di competizione. Atti Soc. it. Ippol. 11, 25-28.
  • Ferlazzo, A., Fazio, E. and Medica, P. (2007) Hormonas y Ejercicio. In: Fisiologia del Ejercicio en Equinos, Ed: F.Boffi, Editorial Inter-Médica S.A.I.C.I., Buenos Aires, República Argentina. pp 153-164.
  • Ferlazzo, A., Fazio, E., Medica, P. and Lindner, A. (1996) Coefficient of variation of and effect of conditioning on concentration of plasma total and free iodothyronines in Thoroughbred horses. Pferdeheilkunde 12, 493-495.
  • Ferlazzo, A., Medica, P., Cravana, C. and Fazio, E. (2009) Endocrine changes after experimental showjumping. Comp. Exerc Physiol. 6, 59-66.
  • Foreman, J.H. and Ferlazzo, A. (1996) Physiological responses to stress in the horse. Pferdeheilkunde 12, 401-404.
  • Garcia, M.C. and Beech, J. (1986) Endocrinologic, hematologic and heart rate changes in swimming horses. Am. J. vet. Res. 47, 2004-2006.
  • Goldfarb, A.H., Hatfield, B.D., Sforzo, G.A. and Flynn, M.G. (1987) Serum beta-endorphin levels during a graded exercise test to exhaustion. Med. Sci. Sports Exerc. 19, 78-82.
  • Gonzáles, O., Gonzáles, E., Sánchez, C., Pinto, J., Gonzáles, I., Enríquez, O., Martínez, R., Filgueira, G. and White, A. (1998) Effect of exercise on erythrocyte beta-adrenergic receptors and plasma concentrations of catecholamines and thyroid hormones in Thoroughbred horses. Equine vet. J. 30, 72-78.
  • Graves, E.A., Schott, II, H.C., Marteniuk, J.V., Refsal, K.R. and Nachreiner, R.F. (2006) Thyroid hormone responses to endurance exercise. Equine vet. J., Suppl. 36, 32-36.
  • Hackney, A.C. and Gulledge, T. (1994) Thyroid hormone response during 8-hour period following aerobic and anaerobic exercise. Physiol. Res. 43, 1-5.
  • Hada, H., Onaka, T., Takahashi, T., Hiraga, A. and Yagi, K. (2003) Effects of novelty stress on neuroendocrine activities and running performance in thoroughbred horses. J. Neuroendocrinol. 15, 638-648.
  • Helmreich, D.L., Crouch, M., Dorr, N.P. and Parfitt, D.B. (2006) Peripheral triiodothyronine (T3) levels during escapable and inescapable footshock. Physiol. Behav. 87, 114-119.
  • Hoffsis, G.F., Murdick, P.W., Tharp, V.L. and Ault, K. (1979) Plasma concentrations of cortisol in the normal horse. Am. J. vet. Res. 31, 1379-1387.
  • Hydbring, E., Nyman, S. and Dahlborn, K. (1996) Changes in plasma cortisol, plasma β-endorphin, heart rate, haematocrit and plasma protein concentration in horses during restraint and use of a naso-gastric tube. Pferdeheilkunde 12, 423-427.
  • Irvine, C.H.G. (1967) Thyroxine secretion rate in the horse under various physiological states. J. Endocr. 39, 313-320.
  • Irvine, C.H.G. and Alexander, S.L. (1994) Factors affecting the circadian rhythm in plasma cortisol concentrations in the horse. Domest. Anim. Endocrinol. 11, 227-238.
  • James, V.H.T., Horner, M.W., Moss, M.S. and Rippon, A.E. (1970) Adrenocortical function in the horse. J. Endocrinol. 48, 319-335.
  • Kurosawa, M., Nagata, S., Takeda, F., Kurosawa, M., Mima, K., Hiraga, A., Kai, M. and Taya, K. (1998) Plasma catecholamine, adrenocorticotropin and cortisol responses to exhaustive incremental treadmill exercise of the Thoroughbred horse. J. equine Sci. 9, 9-18.
  • Lekeux, P., Art, T., Linden, A., Desmecht, D. and Amory, H. (1991) Heart rate, haematological and serum biochemical responses to showjumping. In: Equine Exercise Physiology 3, Eds: S.G.B.Persson, A.Lindholm and L.B.Jeffcott, ICEEP Publications, Davis, California. pp 385-390.
  • Linden, A., Art, T., Amory, H., Desmecht, D. and Lekeux, P. (1991) Effect of 5 different types of exercise, transportation and ACTH administration on plasma cortisol concentration in sport horses. In: Equine Exercise Physiology 3, Eds: S.G.B.Persson, A.Lindholm and L.B.Jeffcott, ICEEP Publications, Davis, California. pp 391-396.
  • Lo, M.J., Kau, M., Chen, Y.H., Tsai, S.C., Chiao, Y.C., Chen, J.J., Liaw, C., Lu, C.C., Lee, B.P., Chen, S.C., Fang, V.S., Ho, L.T. and Wang, P.S. (1998) Acute effects of thyroid hormones on the production of adrenal cAMP and corticosterone in male rats. Am. J. Physiol. 274, E238-E245.
  • McCarthy, R.N., Jeffcott, L.B., Funder, J.W., Fullerton, M. and Clarke, I.J. (1991) Plasma beta-endorphin and adrenocorticotropin in young horses in training. Aust. vet. J. 68, 359-361.
  • Maier, S. (1993) Learned helplessness: relationships with fear and anxiety. In: Stress: From Synapse to Syndrome, Eds: C.Stanford and P.Salmon, Academic Press, London. pp 207-243.
  • Malinowski, K., Shock, E.J., Roegner, V., Rochelle, P., Kearns, C.F., Guirnalda, P. and McKeever, K.H. (2002) Age and exercise training alter plasma beta-endorphin, cortisol, and immune parameters in horses. J. anim. Sci. 80 ( Suppl . 1), 156.
  • Mehl, M.L., Sarkar, D.K., Schott, II, H.C., Brown, J.A., Sampson, S.N. and Bayly, W.M. (1999) Equine plasma β-endorphin concentrations are affected by exercise intensity and time of day. Equine vet. J., Suppl. 30, 567-569.
  • Mehl, M.L., Schott, II, H.C. and Sarkar, D.K. (2000) Effects of exercise intensity and duration on plasma β-endorphin concentrations in horses. Am. J. vet. Res. 61, 969-973.
  • Nagata, S., Takeda, F., Kurosawa, M., Mima, K., Hiraga, A., Kai, M. and Taya, K. (1999) Plasma adrenocorticotropin, cortisol and catecholamines response to various exercises. Equine vet. J., Suppl. 30, 570-574.
  • Panciera, D.L., Hinchcliff, K.W., Olson, J. and Constable, P.D. (2003) Plasma thyroid hormone concentrations in dogs competing in a long-distance sled dog race. J. vet. intern. Med. 17, 593-596.
  • Rone, J.K., Dons, R.F. and Reed, H.L. (1992) The effect of endurance training on serum triiodothyronine kinetics in man: physical conditioning marked by enhanced thyroid hormone metabolism. Clin. Endocrinol. 37, 325-330.
  • Rose, R.J. and Hodgson, D.R. (1994) Haematology and biochemistry. In: The Athletic Horse: Principles and Practice of Equine Sports Medicine, Eds: D.R.Hodgson and R.J.Rose, W.B. Saunders Comp, Philadelphia. pp 63-78.
  • Rudas, P., Rónai, Z. and Bartha, T. (2005) Thyroid hormone metabolism in the brain of domestic animals. Domest. Anim. Endocrinol. 29, 88-96.
  • Sanchez-Franco, F.L., Fernandez, L., Fernandez, G. and Cacicedo, L. (1989) Thyroid hormone action on ACTH secretion. Horm. Metab. Res. 21, 550-552.
  • Sander, M. and Rocker, L. (1988) Influence of marathon running on thyroid hormones. Int. J. Sports Med. 9, 123-126.
  • Snow, D.H., Harris, R.C., MacDonald, I.A., Forster, C.D. and Marlin, J.A. (1992) Effects of high-intensity exercise on plasma catecholamines in the Thoroughbred horse. Equine vet. J. 24, 462-467.
  • Surks, M.I., Goswami, G. and Daniels, G.H. (2005) The thyrotropin reference range should remain unchanged. J. Clin. Endocrinol. Metab. 90, 5489-5496.
  • Terjung, R.J. and Winder, W.W. (1975) Exercise and thyroid function. Med. Sci. Sports 7, 20-26.
  • Thornton, J.R. (1985) Hormonal responses to exercise and training. Vet. Clin. N. Am.: Equine Pract. 1, 477-496.
  • Tucker, D.M., Penland, J.G., Beckwith, B.E. and Sandstead, H.H. (1984) Thyroid function in normals: influences on electroencephalogram and cognitive performance. Psychophysiol. 21, 72-78.