SEARCH

SEARCH BY CITATION

Keywords:

  • horse;
  • stomach;
  • ulcerations;
  • overtraining;
  • exercise

Summary

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

Reasons for performing study: Gastric ulceration can be caused by different pathophysiological mechanisms including dietary factors, psychological stress and exercise. Overtraining is a medical syndrome in performance horses associated with altered hormone levels, altered feed intake, altered behaviour and decreased performance. These components might lead to a higher incidence of gastric ulceration in overtrained horses.

Objectives: To investigate whether the incidence of gastric ulceration is increased in overtrained compared to control horses.

Methods: A longitudinal training study with twelve 1.5 years old Standardbred horses was performed on a treadmill for a total of 32 weeks. Training was divided into 4 periods: (1) acclimatisation (2) training (3) intensified training, and (4) detraining. In period 3, the horses were randomly divided into 2 groups: control (C) and intensified trained group (IT). At the end of each period, gastroscopy was performed in conscious horses after withholding feed for 12 h and water for 6 h using a 3.5 m video gastroendoscope. Lesion scores were assigned to areas of the stomach and graded 1–4. Logistic regression was used for statistical calculations.

Results: Evaluation of the stomach revealed only minor changes (grades 1 or 2) on each occasion. There were no significant differences in gastric lesion scores between groups or periods. Most lesions (70%) were found around the minor curvature. After detraining no lesions (0%) were found in contrast to periods 1 (40%, P = 0.056), 2 (30%) and 3 (30%).

Conclusions: Experimentally-induced overtraining does not increase the incidence of gastric ulceration in normally fed Standardbred horses and detraining appears to reduce gastric ulceration.


Introduction

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

Severe physical exertion has been associated with gastric ulcers and gastrointestinal bleeding in human athletes and in racing Alaskan sled dogs (Choi et al. 2001; Davis et al. 2003). Overtraining syndrome in human athletes, a syndrome caused by imbalance between training intensity and recovery time, has been associated with gastrointestinal disturbances and anorexia (Fry et al. 1991), although as far as we know, no studies performed gastroendoscopies in overtrained or overreached athletes.

In horses, the occurrence of gastric ulceration is associated with many factors, including dietary factors, psychological stress and exercise/training (White et al. 2007). Light exercise may increase the incidence of gastric ulcerations, but an increase of the intensity of training has been shown to further increase the incidence and severity of gastric ulcers (Dionne et al. 2003; White et al. 2007). Overtraining is a medical syndrome in equine athletes associated with altered stress hormone levels (De Graaf-Roelfsema et al. 2007, 2009), altered feed intake/weight loss (McGowan and Whitworth 2008) and decrease in performance (Golland et al. 1999; De Graaf-Roelfsema et al. 2009). Those components might lead to a higher incidence of gastric ulceration in overreached/overtrained horses. In addition, gastric ulcers also adversely affect appetite and physiological indices of performance in horses (Nieto et al. 2009) which might worsen the symptoms of overtraining. To the best of our knowledge, it is not known if gastric ulcerations occur in overtrained horses. We hypothesise that in overtrained horses the incidence and severity of gastric ulcerations will be higher compared to normally trained horses. In order to test our hypothesis we performed an endoscopy of the stomach at several stages during an overtraining study of 32 weeks in a control and a test group.

Materials and methods

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

Animals

Twelve Standardbred geldings were used in this study. They were trained in 2 groups of 6 for logistical reasons. Six horses were trained in 3 pairs of 2 horses per year. Each test horse had its own age-matched control which formed a couple (pair) during the whole session. These individual couples underwent identical daily routines. Horses were aged 20 ± 2 (mean ± s.d.) months with a bodyweight of 368 ± 45 kg (mean ± s.d.) at the beginning of the experiment. The horses had no known history of health and exercise problems and had not previously been involved in any kind of organised exercise or training regimen. The horses were individually housed in box stalls and their diet consisted of grass silage supplemented with concentrated feed and vitamin supplements and met nutrient requirements for maintenance and performance (58 MJ net energy [range 54–66]). Salt blocks and water were available ad libitum. The experiments were approved by the Committee for Animal Welfare at the Faculty of Veterinary Medicine, Utrecht University.

Experimental set-up

Prior to the start of the experiment, the horses were acquainted with the Equine Exercise Laboratory and acclimatised to running on the high-speed treadmill (Mustang 2000)1. The training period consisted of a total of 32 weeks divided into 4 phases as described previously (De Graaf-Roelfsema et al. 2009). At the end of each phase, several tests were performed among them a gastroendoscopy and a standardised exercise test to monitor performance.

Training

All training sessions and exercise tests were performed on a high-speed treadmill. Each training session was preceded by a 30 min warm-up walk in a horse walker followed by an 8 min warm-up on the treadmill, which consisted of 4 min of walking at a speed of 1.6 m/s and 4 min of slow trotting at a speed of 3.0–4.0 m/s (no incline). Each training session ended with a cool down period consisting of a 5 min walk on the treadmill followed by a 30 min walk in the horse walker. During resting days the horses walked for 60 min in a horse walker.

Training intensity was adjusted according to previous published information on a weekly basis to the measured peak HFs (Polar S610)2, during training sessions (De Graaf-Roelfsema et al. 2009). The study was divided into 4 phases after acclimatisation to exercise. The training programme was constructed as follows.

Phase 1 (habituation phase, 4 weeks): Week 1 of phase 1 consisted of 3 times/week exercise at 30% HFest-max for 20–30 min/session, week 2 consisted of 4 times/week exercise at 30% HFest-max for 25–45 min/session, week 3 consisted of 4 times/week exercise at 40% HFest-max for 30–45 min/session and week 4 consisted of 4 times/week exercise at 50% HFest-max for 35–45 min/session.

Phase 2 (normal training phase, 18 weeks): Training in phase 2 consisted of mixed endurance training (ET) and high-intensity interval training (HIT). Days of ET were alternated with HIT. An ET session consisted of continuous trotting for 20–24 min at 60% HFest-max or trotting for 16–18 min at 75% HFest-max. Each HIT session contained either three 3 min bouts or four 2 min bouts of exercise at 80–85% HFest-max interspersed by 3 or 2 min recovery bouts at 60% HFest-max. The horses exercised 4 days/week throughout this training period. We considered that in this phase training could be performed without excessive effort by the horses; therefore, we called this the normal training (NT) phase.

Phase 3 (intensified training phase, 6 weeks): In phase 3, one horse of each couple was randomly selected (by drawing lots) and subjected to an intensified training (IT) programme, whereas the other horse continued training at the volume, intensity and frequency it received in phase 2. The IT regimen consisted of alternating days of HIT and ET as described in phase 2 for 6 days/week during the first 3 weeks. For the last 3 weeks, horses were trained 7 days a week, HIT 4 times and ET 3 times. Exercise intensity during ET was gradually increased to 24–35 min at 60–75% HFest-max. High-intensity exercise gradually increased to five 3 min bouts at 80–85%HFest-max interspersed with 2 min periods at 60% HFest-max or six 2 min bouts at 80–85%HFest-max interspersed with 1 min periods at 60% HFest-max. We anticipated that such a training schedule could be considered as highly intense for the animals.

Phase 4 (reduced training phase, 4 weeks): In phase 4, all horses performed endurance training for 20 min at 60% HFest-max for 3 days and 70% HFest-max for 1 day a week.

Standard exercise test (SET)

Four standardised exercise tests (SETs 1–4) were performed on the final day of each phase to monitor performance. Before the SET started, horses walked for 30 min in the horse walker followed by a warm-up on the treadmill that consisted of 4 min walk (1.6 m/s) and 4 min trotting at 4.5 m/s. Next, after 1 min of additional walking at 1.5 m/s, horses trotted for 20 min at ∼80% HFest-max. Finally, horses were allowed to cool down for 5 min at 1.5 m/s. Heart frequency was monitored constantly with a Polar S610 heart rate meter and continuous ECG monitoring3. In phases 3 and 4, the speed and inclination were not further increased making a comparison between the tests possible. Overtraining was defined as horses that were not able to keep up with the speed of the treadmill during a standardised exercise test and stopped or changed to an energetically more economical gait, the canter.

Gastroendoscopy

Endoscopic examination of the stomach was performed in conscious horses after feed was withheld for 12 h and water for 6 h with a 3.5 m video gastroendoscope (PV-G300)4. During the endoscopic procedure, the stomach was distended by insufflation of air through the endoscope biopsy channel until the squamous and glandular regions of the gastric mucosa were visible. The surface was cleared of feed material by use of a jet of water passed down the biopsy port. The stomach was systematically evaluated and images of the stomach were recorded on videotape. Lesions scores were assigned to areas of the stomach (cardia, squamous mucosa, margo plicatus, glandular body, minor curvature, antrum/pylorus and duodenum) and scored as described by Murray et al. (2001). grade 0= intact epithelium with no apparent mucosal changes; grade 1= mucosal reddening or squamous hyperkeratosis; grade 2= small single or multifocal lesions; grade 3= large single or multifocal lesions or extensive superficial lesions; grade 4= extensive lesions with apparent deep ulceration.

Statistics

The variable stomach ulcer was analysed using a logistic regression with random horse effects and with group, period and their interaction as fixed effects (R version 2.10.1, General Public License). The significance of differences in trotting time during SET 3 and SET 4 between both groups was assessed by the independent t test. P value <0.05 was considered significant.

Results

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

Because of injury, 2 horses (1 control and 1 IT from the same pair) were not able to complete the training. Analysis is therefore based on the remaining 10 horses.

The SETs were performed throughout the experiment to monitor performance. Results are published before (de Graaf-Roelfsema et al. 2009). Regarding the IT group, horses maintained trotting at high speeds during SET 3 for 16.1 ± 2.3 min compared with 19.8 ± 0.4 min (P = 0.012) in control horses. IT horses started galloping frequently at the beginning of SET 3 despite humane encouragement to trot or stopped. As a consequence, the mean duration of trotting during SET 3 was decreased significantly by 19% in the IT group as compared with control horses. In addition, after 4 weeks of detraining the IT horses still showed a reduction on the average in treadmill trotting-time-to-fatigue during the standardised exercise test. (IT 16.2 ± 2.3 vs. C 19.7 ± 0.76, P = 0.012).

There were no significant differences in presence of gastric lesions between groups (C vs. IT) or periods (1–4) (Table 1). After detraining, no lesions (0%) were found in contrast to period 1 (40%), period 2 (30%) and period 3 (30%). Most lesions (70%) were found around the minor curvature (Table 2). Evaluation of the stomach revealed only minor changes (grades 1 or 2) following the different training phases (Table 3). When lesions were found within a horse it was at one location only at a time; there was one exception after phase 1 one horse showed ulcerations grade 2 at the margo plicatus and lesser curvature. Two horses showed lesions at one time during the different phases. Four horses showed gastric lesions 2 times during the different phases.

Table 1. Number of horses (%) (5 control [C] and 5 intensified trained [IT]) with and without gastric lesions after different phases of training. Horses were randomly divided in C and IT at the end of phase 2
PhaseWith lesionsWithout lesions
CITCIT
110304020
220103040
320103040
4005050
Table 2. Overall localisation of the gastric lesions after different phases of training in horses suffering from gastric lesions
LocalisationPhase 1Phase 2Phase 3Phase 4
Cardia0000
Squamous mucosa1000
Margo plicatus1000
Glandular mucosa0000
Minor curvature2330
Pylorus1000
Duodenum0000
Table 3. Overall severity of the gastric lesions expressed in number of horses after different phases of training
PhaseGrade 1Grade 2Grade 3Grade 4
11300
23000
32100
40000

Discussion

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

The drop in performance seen in the current study is similar with the reduction on the average in treadmill run-time-to-fatigue by 14% as reported in horses by others (Golland et al. 1999). Extending the trot can have profound energetic requirements that could limit performance as compared with cantering (Wickler et al. 2002). Given the fact that Standardbred horses are bred for trotting and, taking into account the lower energetic costs of cantering, the intensified group clearly showed a loss of performance, indicative for overtraining since recovery did not succeed within 4 weeks of detraining (Kreider et al. 1998; Lehmann et al. 1999). As previously published the intensively trained horses in this study showed changes in behaviour and derangements in hormonal secretions after the intensified training phase which is also indicative of overtraining (de Graaf-Roelfsema et al. 2009).

This study investigated the hypothesis that in overtrained horses the incidence and severity of gastric ulcerations would be higher compared to normally trained horses. Despite the limitations of the study, due to the small number of horses used and absence of gastroendoscopy at the start of the experiment, such hypothesis does not seem supported by our data. This study shows that overtrained horses have gastric ulcers but not more, or more severe, than control horses. It appeared that the lesions do not progress during a further increase in training intensity or volume as occurred during phase 3. Interestingly, even if the results were not statistically significant, it seems there may be a trend toward decreased gastric ulceration in horses that are detraining (P = 0.06).

Exercise is considered a risk factor to ulceration of the squamous mucosa (Orsini et al. 2009). Exercise is supposed to decrease gastric motility or increase intragastric pressure as a result of action of the abdominal muscles or increased respiratory effort leading to a disruption of the normally occurring dorsoventral pH gradient (Bell et al. 2007). The increase in abdominal pressure during exercise causes compression of the stomach, which in turn leads to exposure of the squamous portion of the stomach to hydrochloric acid and organic acids (volatile, fatty and bile acids) (Lorenzo-Figueras and Merritt 2002). In this study, 92% of the gastric lesions were localised in the gastric squamous mucosa with most lesions localised along the lesser curvature which is in accordance with other studies reporting a higher number and greater severity of ulcers seen at the lesser curvature in trained horses (Murray and Eichhorn 1996; Dionne et al. 2003; Bell et al. 2007).

It is known that gastric ulcers can develop quickly in horses in training and 8 days was enough to induce gastric ulcers in a high percentage of horses engaged in various exercise regimens (light to heavy) suggesting that long-term intensive training regimens are not required for ulcer development (White et al. 2007). In this experiment, horses showed gastric lesions after 4 weeks of light training and accommodation to the training environment. Unfortunately, no endoscopy was performed at the start of the experiment and therefore it is not certain that gastric ulcerations developed after start of the experiment due to the training. McClure et al. (2005) showed that keeping horses in unfamiliar surroundings combined with performing light exercise is enough to develop mild gastric ulceration within 5 days. Therefore, it is possible that the stall confinement in unfamiliar surroundings before the start of the experiment influenced the incidence of gastric lesions at the end of phase 1.

The lack of progression of gastric lesion severity with increase in training intensity and volume was unexpected because earlier studies indicated that increased incidence of ulceration and worsening of ulceration grade progressed as horses progressed through training and racing (Dionne et al. 2003; Orsini et al. 2009). In contrast, the acclimatisation period seem to be the period with the highest incidence of lesions and the highest incidence of more severe lesions. Probably, the habituation to training on the treadmill and experimental circumstances had more influence on development of gastric ulcers than a further increase in training intensity and volume.

Stress is considered a risk factor for developing gastric ulceration. Not every stressor will lead to gastric ulceration and multiple animal models of stress have been used to mimic stressful events or chronic stress in order to unravel the effects of stress on gastric mucosa (Caso et al. 2008). It is well known from studies in laboratory animals that different stressors can increase gastrin and histamine plasma levels, enhance the production of gastric acid and reduce gastric mucosal blood flow, leading to the development of acute gastric lesions (Caso et al. 2008). In horses, treadmill exercise has an effect upon the serum gastrin response to a meal in the horse, but so far the relationship of this finding to the development of gastric ulcer disease is unknown (Furr and Kronfeld 1994). An organism develops defence and adaptive mechanisms in order to ensure survival in response to stress. Some adaptive responses directed towards the restoration of gastrointestinal functional homeostasis and physical integrity have been described including the sensory neurons of the enteric nervous system (their role in enhancing mucosal defence and regulation of mucosal blood flow) and the hormones vasopressin and prolactin which seem to induce protective mechanisms, although the responsible mechanisms are not understood (Caso et al. 2008).

Overtraining is a stress-related disease probably caused by a neuro-endocrine imbalance. Derangement of hormonal secretion has been previously described for overtrained horses (De Graaf-Roelfsema et al. 2007, 2009; McGowan and Whitworth 2008) but the influence of these alterations on gastric mucosa is not known. This is the first study to perform gastroscopy in overtrained horses and to find that early overtraining is not associated with increased incidence or severity of gastric lesions. This study underlines that exercise plays a role in the development of EGUS, but probably not the most important. Psychological stressors such as changes in environment and feeding regimen seem to be more important than training stress. Further research is needed to determine if training stress induces adapting processes in the stomach in horses.

Acknowledgements

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

We would like to thank all people of the Department of Equine Sciences, especially A. Klaarenbeek and H. van Voorst for training of the horses and J. van den Broek for the statistical analysis.

Manufacturers' addresses

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

1 Kagra, Graber AG, Fahrwangen, Switzerland.

2 Polar Electro Oy, Kempele, Finland.

3 Cardio Perfect Stress 4.0, Cardio Perfect Inc, Atlanta, Georgia, USA.

4 Xion Medical, Berlin, Germany.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Conflicts of interest
  9. Manufacturers' addresses
  10. References
  • Bell, R.J.W., Mogg, T.D. and Kingston, J.K. (2007) Equine gastric ulcer syndrome in adult horses: a review. N. Z. vet. J. 55, 1-12.
  • Caso, J.R., Leza, J.C. and Menchen, L. (2008) The effects of physical and psychological stress on the gastro-intestinal tract: lessons from animal models, Curr. Mol. Med. 8, 299-312.
  • Choi, S.C., Choi, S.J., Kim, J.A., Kim, T.H., Nah, Y.H., Yazaki, E. and Evans, D.F. (2001) The role of gastrointestinal endoscopy in long-distance runners with gastrointestinal symptoms. Eur. J. Gastroenterol Hepatol 13, 1089-1094.
  • Davis, M.S., Willard, M.D., Nelson, S.L., Mandsager, R.E., McKiernan, B.S., Mansell, J.K. and Lehenbauer, T.W. (2003) Prevalence of gastric lesions in racing Alaskan sled dogs. J. Vet. Intern. Med. 17, 311-314.
  • De Graaf-Roelfsema, E., Keizer, H.A., Van Breda, E., Wijnberg, I.D. and Van Der Kolk, J.H. (2007) Hormonal responses to acute exercise, training and overtraining. A review with emphasis on the horse. Vet. Q. 29, 82-101.
  • De Graaf-Roelfsema, E., Veldhuis, P.P., Keizer, H.A., Van Ginneken, M.M., Van Dam, K.G., Johnson, M.L., Barneveld, A., Menheere, P.P., Van Breda, E., Wijnberg, I.D. and Van Der Kolk, J.H. (2009) Overtrained horses alter their resting pulsatile growth hormone secretion. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R403-R411.
  • Dionne, R.M., Vrins, A.A. and Doucet, M.Y. (2003) Gastric ulcers in standardbred racehorses: prevalence, lesion description, and risk factors. J. vet. intern. Med. 17, 218-222.
  • Fry, R.W., Morton, A.R. and Keast, D. (1991) Overtraining in athletes. An update. Sports Med. 12, 32-65.
  • Furr, M., Taylor, L. and Kronfeld, D. (1994) The effects of exercise training on serum gastrin responses in the horse. Cornell Vet. 84, 41-45.
  • Golland, L.C., Evans, D.L., Stone, G.M., Tyler-McGowan, C.M., Hodgson, D.R. and Rose, R.J. (1999) Plasma cortisol and β-endorphin concentrations in trained and over-trained Standardbred racehorses. Pflugers. Arch. 439, 11-17.
  • Kreider, R., Fry, A.C. and O'Toole, M.L. (1998) Overtraining in sport: terms, definitions, and prevalence. In: Overtraining in Sport, Eds: R.Kreider, A.C.Fry and M.L.O'Toole, Human Kinetics, Champaign. pp vii-vix.
  • Lehmann, M., Foster, C., Gastmann, U., Keizer, H. and Steinacker, J.M. (1999) Definition, types, symptoms, findings, underlying mechanisms, and frequency of overtraining and overtraining syndrome. In: Overload, Performance Incompetence, and Regeneration in Sport, Eds: M.Lehmann, C.Fostee, U.Gastmann, H.Keizee, and J.M.Steinacker, Kluwer Academic/Plenum Publishers, New York, Boston, Dordrecht, London, Moscow. pp 1-7.
  • Lorenzo-Figueras, M. and Merritt, A.M. (2002) Effects of exercise on gastric volume and pH in the proximal portion of the stomach of horses. Am. J. vet. Res. 63, 1481-1487.
  • McGowan, C.M. and Whitworth, D.J. (2008) Overtraining syndrome in horses. Comp. Exerc. Phys. 5, 57-65.
  • Murray, M.J. and Eichhorn, E.S. (1996) Effects of intermittent feed deprivation, intermittent feed deprivation with ranitidine administration, and stall confinement with ad libitum access to hay on gastric ulceration in horses. Am. J. vet. Res. 57, 1599-1603.
  • Murray, M.J., Nout, Y.S. and Ward, D.L. (2001) Endoscopic findings of the gastric antrum and pylorus in horses: 162 cases (1996–2000). J. vet. intern. Med. 15, 401-406.
  • McClure, S.R., Carithers, D.S., Gross, S.J. and Murray, M.J. (2005) Gastric ulcer development in horses in a simulated show or training environment. J. Am. Vet. Med. Assoc. 227, 775-777.
  • Nieto, J.E., Snyder, J.R., Vatitas, N.J. and Jones, J.H. (2009) Effect of gastric ulceration on physiologic responses to exercise in horses. Am. J. vet. Res. 70, 787-795.
  • Orsini, J., Hackett, E. and Grenager, N. (2009) The effect of exercise on equine gastric ulcer syndrome in the thoroughbred and standardbred athlete. J. equine vet. Sci. 29, 167-171.
  • White, G., McClure, S.R., Sifferman, R., Holste, J.E., Fleishman, C., Murray, M.J. and Cramer, L.G. (2007) Effects of short-term light to heavy exercise on gastric ulcer development in horses and efficacy of omeprazole paste in preventing gastric ulceration. J. Am. vet. med. Ass. 230, 1680-1682.
  • Wickler, S.J., Hoyt, D.F., Cogger, E.A. and McGuire, R. (2002) The cost of transport in an extended trot. Equine vet. J., Suppl. 34, 126-130.