Abstract
The objectives of this study were to determine the prevalence rates and risk factors for equine glandular gastric disease (EGGD) and equine squamous gastric disease (ESGD) in a population of 63 polo horses in competition. The prevalence of EGGD grade ≥ 1 was 69% and EGGD ≥ 2 was 31%. The prevalence of ESGD grade ≥ 1 was 54% and grade ≥ 2 was 37%. The risk factors retained in the final multivariable models were years of experience in polo competition for EGGD grade ≥ 1 and for grade ≥ 2, with decreased experience being associated with EGGD and weekly exercise duration and non-steroidal anti-inflammatory drug (NSAID) use being associated with ESGD grade ≥ 1. Decreasing weekly exercise duration was the only risk factor associated with ESGD grade ≥ 2. Equine gastric disease was common in this population of polo horses and the amount of experience and weekly exercise duration were related to the risk of disease.
Résumé
Prévalence de la maladie gastrique glandulaire et squameuse des équidés et facteurs de risque chez les chevaux de polo. Les objectifs de cette étude consistaient à déterminer les taux de prévalence et les facteurs de risque pour la maladie gastrique glandulaire équine (MGGE) et la maladie gastrique squameuse équine (MGSE) dans une population de 63 chevaux de polo de compétition. La prévalence de la MGGE de grade ≥ 1 était de 69 % et de la MGGE ≥ 2 était de 31 %. La prévalence de la MGSE de grade ≥ 1 était de 54 % et de grade ≥ 2 était de 37 %. Les facteurs de risque conservés dans les modèles multivariables finaux étaient des années d’expérience dans les compétitions de polo pour la MGGE de grade ≥ 1 et de grade ≥ 2, et une expérience réduite était associée à la MGGE et la durée de l’exercice hebdomadaire et l’usage d’anti-inflammatoires non stéroïdiens (AINS) étaient associés à la MGSE de grade ≥ 1. La réduction de l’exercice hebdomadaire était le seul facteur de risque associé à la MGSE de grade ≥ 2. La maladie gastrique équine est commune dans cette population de chevaux de polo et la quantité d’expérience et la durée de l’exercice hebdomadaire étaient associées au risque de maladie.
(Traduit par Isabelle Vallières)
Introduction
Equine gastric ulcer syndrome is a term that includes lesions within both the squamous region [equine squamous gastric disease (ESGD)] and the glandular region [equine glandular gastric disease (EGGD)] (1). Both squamous and glandular gastric lesions are common in performance horses, with the prevalence of ESGD ranging from 17% to 100% (2–13) and the prevalence of EGGD ranging from 16% to 65% (1,3,11,14–16). The different prevalences identified in these studies suggest that risk factors may differ for ESGD and EGGD. Furthermore, breed, performance discipline, management, or a combination of factors may influence risk of disease.
Previous studies investigating risk factors for gastric lesions have focused on ESGD. A high grain diet was associated with increased risk of ESGD in 1 epidemiological study (17), a finding that is supported by a prospective study demonstrating that a high starch diet can induce ESGD (18). Training and competition also appear to be risk factors for ESGD (2,3,5–7,14,15). The combination of training and a high grain diet has been shown to induce ESGD (19). However, the role of other management factors, such as pasture turnout or forage type, remains unclear (1,13,20–22).
In contrast, there are few studies evaluating risk factors for EGGD. No association of age, breed, or gender with EGGD was discovered in one study (16), while another study found the Warmblood breed had an increased risk of EGGD (23). Additional epidemiological studies may identify dietary and management risk factors for different breeds and performance disciplines that contribute to the development of EGGD and ESGD.
Polo horses represent a unique equine performance population as they are often housed and trained in groups, rather than individually. The objectives of this study were to establish the prevalence and severity of gastric disease (ESGD and EGGD) and to identify risk factors for ESGD and EGGD in polo horses.
Materials and methods
Study population
This study was approved by the University of Calgary’s Veterinary Sciences Animal Care Committee (#AC14-003). Horses were recruited by a referring veterinarian (CC) who routinely provided veterinary care to 2 polo clubs in the Calgary area. In order to be included in the study, horses needed to be in training for or competing in polo. Horses were excluded if they had received any anti-ulcer medications (e.g., omeprazole, misoprostol, sucralfate, H2 antagonists) within 4 wk prior to gastroscopy. Sixty-three polo horses from 9 barns were examined by endoscopy from June to August 2014. No horses were excluded from the study; however, the authors did not track whether all eligible horses from a barn were offered for inclusion in the study.
Gastroscopy and gastric disease scoring
Before examination, horses were fasted for 12 to 16 h, sedated with detomidine (Dormosedan; Zoetis, New Jersey, USA), 0.01 to 0.02 mg/kg body weight (BW), IV, and examined with a 3-m endoscope (Karl Storz, Tuttlingen, Germany). Gastric lesions (EGGD and ESGD) were graded on a modified 4-point scale by 2 investigators (HEB, HM) at the time of endoscopy, as previously described (24). All of the types of EGGD including hyperemic, hemorrhagic, fibrinosuppurative, ulcerated; depressed, flat, and raised were considered.
Risk factor questionnaire
A questionnaire was developed through discussion and examination of the literature. Trainers completed a separate questionnaire for each enrolled horse under their care. The questionnaire included questions on signalment (age, gender, breed), medical history (previous medical conditions and treatments), exercise and performance history (exercise frequency and duration, number of years competing, performance level), dietary history (including type of feed and frequency of feedings), and management (duration of time at current barn, housing and turnout type and duration). The questionnaire is available on request from the corresponding author.
Statistical analysis
A Chi-square test was used to determine the relationship between the presence of ESGD (grade ≥ 2) and EGGD (grade ≥ 1 or grade ≥ 2).
Results from the questionnaire were used to evaluate risk factors for ESGD and EGGD. After a preliminary review of the data, several continuous variables were categorized for analysis because of sparse data. Based on the median value for the variable:
total exercise minutes per week was categorized into > 270 or ≤ 270 min/wk;
exercise intensity was classified as high/very high or moderate/low;
games per month was categorized into < 10 or ≥ 10;
level of performance was categorized into < 6 goal or > 6 goal;
grain feeding was categorized as < 1 or ≥ 1 times/d;
hay type was categorized into grass or other;
hay frequency was categorized as ≥ 3 or < 3 times/d;
time at current barn was categorized into ≤ 2 or > 2 mo; and
turnout was categorized as ≤ 6 or > 6 h/d.
Because of small numbers of non-Thoroughbred or Thoroughbred-cross horses (n = 2), breed was not included in the model.
For the risk factor analysis, 4 outcomes were explored: i) EGGD ≥ 1 versus 0; ii) EGGD ≥ 2 versus < 2; iii) ESGD ≥ 1 versus < 0; and, iv) ESGD ≥ 2 versus < 2. Associations between risk factors and the outcomes of EGGD and ESGD were assessed using logistic regression (SPSS; IBM Corporation, Armonk, New York, USA). A univariable logistic regression analysis was performed for all independent variables. Independent variables with P < 0.10 in the univariable logistic regression analysis were considered for the multivariable logistic regression analysis. Independent variables eligible for entry into the model were assessed for collinearity (Pearson or Spearman rank correlation coefficient for continuous and dichotomous variables, respectively). Collinearity was considered present if correlation coefficients were > 0.8. When collinearity was present, multiple models were constructed and only 1 of the collinear variables was included in each model. Aikeke’s information criterion (AIC) was used to evaluate which model best fit the data, and the model with the lowest AIC was retained as the final model. Because horses were clustered by barn, barn was offered as a fixed effect. Backward elimination was used to remove variables with P > 0.05. Confounding of remaining variables was assessed by observing changes > 30% in the remaining coefficients.
Results
Two horses had incomplete examination of the glandular stomach due to residual feed in the stomach; these 2 horses did not have an EGGD score assigned and were excluded from EGGD analysis but included in the ESGD analysis.
Breeds represented included 1 mixed breed (Quarter horse × Thoroughbred), 1 Criollo, 1 Paint, 3 Argentine polo ponies, and 57 Thoroughbred horses. There were 22 geldings and 41 mares. Mean age [± standard deviation (SD)] was 12 ± 5 y. One horse had a history of colic and 1 horse had a history of chronic diarrhea. There was no history of respiratory or gastric disease in any horse. No horse was receiving any treatments for gastric disease. Medications administered included non-steroidal anti-inflammatory drugs (NSAIDs; n = 11, phenylbutazone, n = 7; firocoxib, n = 4, and glucosamine, n = 6). Supplements fed included electrolytes (n = 22), mineral mix (n = 9), and psyllium (n = 4). No supplements with identifiable antacid properties were fed.
Overall prevalence of EGGD and ESGD is presented in Table 1. There was no association between ESGD grade ≥ 2 and either EGGD grade ≥ 1 (P = 0.59) or EGGD grade ≥ 2 (P = 0.09). Results of the univariable analysis for ESGD variables with P < 0.05 are reported in Table 2, and results of the univariable analysis for EGGD variables with P < 0.05 are reported in Table 3. As there was no significant clustering by barn when evaluating EGGD (P > 0.3) or ESGD (P > 0.8), effect of barn was not included in the final multivariable model.
Table 1.
Prevalence of gastric disease in 63 polo horses.
| Grade | ESGD | EGGD |
|---|---|---|
| ≥ 1 | 54% | 69% |
| ≥ 2 | 37% | 31% |
ESGD — equine squamous gastric disease; EGGD — equine glandular gastric disease.
Table 2.
Univariable analysis of factors associated with ESGD grade ≤ 1 or ESGD ≤ 2 (P ≤ 0.05).
| Characteristic | ESGD grade ≥ 1 % affected (affected/total) or Mean ± SD | Odds ratio | P-value | ESGD Grade ≥ 2 % affected (affected/total) or Mean ± SD | Odds ratio | P-value |
|---|---|---|---|---|---|---|
| Years owned | Unaffected: 3.1 ± 1.9 | Referent | 0.003 | — | ||
| Affected: 2.4 ± 1.3 | 2.0 | |||||
| Time at current barn | ||||||
| ≤ 2 mo | 46% (18/39) | Referent | — | |||
| > 2 mo | 85% (11/13) | 6.4 | 0.03 | — | ||
| Exercise duration (min/wk) | ||||||
| > 270 | 18% (5/28) | Referent | < 0.001 | 7% (2/28) | Referent | < 0.001 |
| ≤ 270 | 83% (29/35) | 20 | 60% (21/35) | 20 | ||
| Travelling | ||||||
| No | 31% (11/35) | Referent | 23% (8/35) | Referent | ||
| Yes | 79% (19/24) | 8.3 | 0.001 | 50% (12/24) | 3.4 | 0.03 |
| Hay frequency | ||||||
| ≥ 3 times/d | 38% (14/37) | Referent | — | |||
| < 3 times/d | 77% (20/26) | 5.6 | 0.003 | — | ||
| Bran | ||||||
| Yes | 28% (5/18) | Referent | — | |||
| No | 64% (29/45) | 4.8 | 0.01 | — | ||
| Electrolytes | ||||||
| Yes | 36% (8/22) | Referent | — | |||
| No | 63% (26/41) | 3.0 | 0.04 | — | ||
| Housing: paddock | ||||||
| Yes | 42% (15/36) | Referent | 0.03 | 25% (9/36) | Referent | |
| No | 70% (19/27) | 3.3 | 52% (14/27) | 1.5 | 0.03 | |
| Turnout duration | ||||||
| ≤ 6 h | 19% (3/16) | Referent | 6% (1/16) | Referent | ||
| > 6 h | 66% (31/47) | 8.4 | 0.003 | 46% (22/47) | 13.2 | 0.02 |
| NSAID use | ||||||
| Yes | 18% (2/11) | Referent | — | |||
| No | 62% (32/52) | 7.1 | 0.02 | — | ||
Table 3.
Univariable analysis of factors associated with EGGD grade ≤ 1 or EGGD ≤ 2 (P ≤ 0.05).
| Characteristic | EGGD grade ≥ 1 affected/total or Mean ± SD | Odds ratio | P-value | EGGD grade ≥ 2 affected/total or Mean ± SD | Odds ratio | P-value |
|---|---|---|---|---|---|---|
| Years playing | Unaffected: 9.4 ± 5.0 | Referent | 0.02 | Unaffected: 8.6 ± 5.1 | Referent | 0.03 |
| Affected: 5.7 ± 4.1 | 1.2 | Affected: 4.5 ± 2.2 | 1.3 | |||
| Electrolytes | ||||||
| Yes | — | 50% (11/22) | 3.9 | |||
| No | — | 21% (8/39) | Referent | 0.02 | ||
| Housing: pasture | ||||||
| Yes | 42% (11/26) | Referent | — | |||
| No | 69% (24/35) | 2.9 | 0.04 | — | ||
In the multivariable analysis for ESGD grade ≥ 1, the risk factors that remained in the model were exercise minutes per wk and NSAID use, with horses exercised ≤ 270 min per wk having an increased odds of ESGD grade ≥ 1 [odds ratio (OR) = 32.8; 95% confidence interval (CI) = 6.9 to 155.9; P < 0.0001] and absence of NSAID use associated with an increased odds of ESGD grade ≥ 1 (OR = 15.4; 95% CI: 1.9 to 124.8; P = 0.009). In the multivariable model for ESGD grade ≥ 2, decreasing exercise duration was associated with an increased odds of ESGD grade ≥ 2 (OR = 19.5; 95% CI: 3.8 to 98.7; P = 0.0005). In the multivariable model for EGGD, each 1 y decrease in years playing polo was associated with increased odds of EGGD ≥ 1 (OR = 1.2; 95% CI: 1 to 1.4; P = 0.04) and EGGD ≥ 2 (OR = 1.3; 95% CI: 1 to 1.7; P = 0.04).
Discussion
This study indicates that gastric squamous and glandular disease prevalence among training and competing polo horses differs from those typically observed in racing Thoroughbreds, with higher risk of EGGD and lower risk of ESGD (2,3,20). This suggests that factors associated with performance discipline may play a role in gastric disease formation. There are several ways in which management may differ between previous reports of racing Thoroughbreds and the polo horses of the present study. For example, a previous study reported that turnout in groups and training at the site of housing significantly reduced odds of ESGD (13). The polo horses herein were frequently housed in groups and trained on-site (personal observations), which may have contributed to the lower prevalence observed. Furthermore, polo horses are generally older than racehorses, which may influence the formation of squamous lesions. One study reported differences in squamous mucosal response to VFAs in older compared to younger adult horses, which may alter risk of ESGD (25).
In this study population, duration of exercise and absence of NSAID use were associated with ESGD grade ≥ 1, while duration of exercise was the only factor associated with ESGD grade ≥ 2. Surprisingly, in both models, horses that were exercised less had an increased risk of ESGD. This is in contrast to previous studies which reported that increased racing and training lead to increased risk of ESGD (2,19). This may in part be due to the different type and intensity of exercise training or changes in feeding practices prior to training associated with racing compared to polo. In humans, gastric ulcers are not consistently associated with physical activity, and activity has been reported to be protective against duodenal ulcer in men (26). The negative association between NSAID use and gastric disease formation should be interpreted cautiously, because multiple prior experimental studies have suggested that NSAIDs may induce gastric disease, particularly glandular disease (27–33). However, 2 cross-sectional studies in Thoroughbreds did not demonstrate an association between NSAIDs use and squamous disease (2,4) or glandular disease (2). Dose and duration of NSAID use, type of NSAID used, and the potential interaction between NSAID use and other management factors may influence the differences observed among field and experimental studies.
Of the 11 horses receiving NSAIDs in the present study, 1 received phenylbutazone twice daily (dose unknown) for 10 d, 6 received phenylbutazone “as needed” (dose unknown), and 4 received firocoxib (57 mg) daily. Intermittent dosing of phenylbutazone is likely to have a lower risk of inducing gastric disease, compared to daily administration. Furthermore, COX-2 selective NSAIDs may be safer for the gastric mucosa than phenylbutazone. A prior study in horses suggested that treatment with phenylbutazone increased gastric permeability over time, while the COX-2 preferential NSAID, meloxicam, did not (34). However, whether COX-2 selective NSAIDs such as firocoxib, are safer for the gastric mucosa remains unknown. It must also be considered that this counter-intuitive finding may be spurious, given the relatively small sample size of this study.
The only risk factor that remained in the final multivariable analysis for EGGD (grade ≥ 1 or grade ≥ 2) was years playing polo. For every year of less experience playing polo, odds of having EGGD increased. This suggests that experience may be protective against gastric glandular disease. It has been previously demonstrated that horses with competition experience may have lower basal cortisol at a horse show or in response to a jumping event (35,36). In humans, psychological stress has been proposed to contribute to peptic ulcer disease (37,38). As experience in the discipline increases, horses may become accustomed to training and competition practices, which may limit stress response and thus development of glandular disease. It is also possible that horses that are more experienced may be able to train for the same duration of time or at the same perceived intensity with less effort.
In this study, risk factors identified differed between the 2 types of gastric disease; there was no relationship between presence of ESGD and presence of EGGD. Previous studies in Thoroughbreds and sport horses have yielded conflicting results regarding the association between squamous and glandular disease (16,39). Taken together, these findings highlight the importance of considering risk factors for ESGD and EGGD separately.
There are several limitations to this study. One limitation was the recruitment strategy, which may have led to increased participation from barns with a higher prevalence of gastric disease. Furthermore, only a small number of horses participated in the study, and a large number of management factors were assessed, which may have led to a Type I or Type II error. The final multivariable models either had confidence intervals that were very close to overlapping 1 (i.e., EGGD models) or had very wide confidence intervals (i.e., ESGD models), which limits our confidence in applying these models to a larger population. Inclusion of additional horses in the study may have allowed for improved multivariable models.
This study provides new information on potential risk factors for squamous and glandular disease in polo horses. Decreasing weekly exercise duration was associated with ESGD, while decreased experience was associated with EGGD. Additional studies, such as prospective cohort or randomized clinical trials with larger numbers of Thoroughbred horses from various disciplines, may help to clarify the contribution of different management practices to equine glandular and squamous gastric disease.
Acknowledgment
We are grateful to Grace Kwong for assistance with statistical analysis. CVJ
Footnotes
Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.
References
- 1.Sykes B, Hewetson M, Hepburn R, Luthersson N, Tamzali Y. European College of Equine Internal Medicine Consensus Statement — Equine gastric ulcer syndrome in adult horses. J Vet Intern Med. 2015;29:1288–1299. doi: 10.1111/jvim.13578. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Murray M, Schusser G, Pipers F, Gross SJ. Factors associated with gastric lesions in Thoroughbred racehorses. Equine Vet J. 1996;28:368–374. doi: 10.1111/j.2042-3306.1996.tb03107.x. [DOI] [PubMed] [Google Scholar]
- 3.Begg L, O’Sullivan C. The prevalence and distribution of gastric ulceration in 345 racehorses. Aust Vet J. 2003;81:199–201. doi: 10.1111/j.1751-0813.2003.tb11469.x. [DOI] [PubMed] [Google Scholar]
- 4.Vatistas N, Snyder J, Carlson G, et al. Cross-sectional study of gastric ulcers of the squamous mucosa in Thoroughbred racehorses. Equine Vet J. 1999;31(S29):34–39. doi: 10.1111/j.2042-3306.1999.tb05166.x. [DOI] [PubMed] [Google Scholar]
- 5.Rabuffo TS, Orsini JA, Sullivan E, Engiles J, Norman T, Boston R. Associations between age or sex and prevalence of gastric ulceration in Standardbred racehorses in training. J Am Vet Med Assoc. 2002;221:1156–1159. doi: 10.2460/javma.2002.221.1156. [DOI] [PubMed] [Google Scholar]
- 6.Dionne RM, Vrins A, Doucet MY, Pare J. Gastric ulcers in standardbred racehorses: Prevalence, lesion description, and risk factors. J Vet Intern Med. 2003;17:218–222. doi: 10.1111/j.1939-1676.2003.tb02437.x. [DOI] [PubMed] [Google Scholar]
- 7.Jonsson H, Egenvall A. Prevalence of gastric ulceration in Swedish Standardbreds in race training. Equine Vet J. 2006;38:209–213. doi: 10.2746/042516406776866390. [DOI] [PubMed] [Google Scholar]
- 8.Murray M, Grodinsky C, Anderson C, Radue P, Schmidt G. Gastric ulcers in horses: A comparison of endoscopic findings in horses with and without clinical signs. Equine Vet J. 1989;21:68–72. doi: 10.1111/j.2042-3306.1989.tb05659.x. [DOI] [PubMed] [Google Scholar]
- 9.McClure S, Glickman L, Glickman N. Prevalence of gastric ulcers in show horses. J Am Vet Medical Assoc. 1999;215:1130–1133. [PubMed] [Google Scholar]
- 10.Hartmann AM, Frankeny RL. A preliminary investigation into the association between competition and gastric ulcer formation in non-racing performance horses. J Equine Vet Sci. 2003;23:560–561. [Google Scholar]
- 11.Luthersson N, Nielsen K, Harris P, Parkin T. The prevalence and anatomical distribution of equine gastric ulceration syndrome (EGUS) in 201 horses in Denmark. Equine Vet J. 2009;41:619–624. doi: 10.2746/042516409x441910. [DOI] [PubMed] [Google Scholar]
- 12.Niedźwiedź A, Kubiak K, Nicpoń J. Endoscopic findings of the stomach in pleasure horses in Poland. Acta Vet Scand. 2013;7:55. doi: 10.1186/1751-0147-55-45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Lester GD, Robertson I, Secombe C. Risk factors for gastric ulceration in Thoroughbred racehorses. Rural Research and Development Corporation; Government of Australia: May, 2008. [Google Scholar]
- 14.Nieto JE, Snyder JR, Beldomenico P, Aleman M, Kerr JW, Spier SJ. Prevalence of gastric ulcers in endurance horses–A preliminary report. Vet J. 2004;167:33–37. doi: 10.1016/j.tvjl.2003.09.005. [DOI] [PubMed] [Google Scholar]
- 15.Tamzali Y, Marguet C, Priymenko N, Lyazrhi F. Prevalence of gastric ulcer syndrome in high-level endurance horses. Equine Vet J. 2011;43:141–144. doi: 10.1111/j.2042-3306.2010.00129.x. [DOI] [PubMed] [Google Scholar]
- 16.Hepburn R. Endoscopic examination of the squamous and glandular gastric mucosa in sport and leisure horses: 684 horses (2005–2011). Proceedings of the 11th International Equine Colic Research Symposium; Dublin, Ireland. July 7–10, 2014. [Google Scholar]
- 17.Luthersson N, Nielsen K, Harris P, Parkin T. Risk factors associated with equine gastric ulceration syndrome (EGUS) in 201 horses in Denmark. Equine Vet J. 2009;41:625–630. doi: 10.2746/042516409x441929. [DOI] [PubMed] [Google Scholar]
- 18.Frank N, Andrews FM, Elliott SB, Lew J. Effects of dietary oils on the development of gastric ulcers in mares. Am J Vet Res. 2005;66:2006–2011. doi: 10.2460/ajvr.2005.66.2006. [DOI] [PubMed] [Google Scholar]
- 19.Vatistas N, Sifferman R, Holste J, Cox J, Pinalto G, Schultz K. Induction and maintenance of gastric ulceration in horses in simulated race training. Equine Vet J. 1999;31:40–44. doi: 10.1111/j.2042-3306.1999.tb05167.x. [DOI] [PubMed] [Google Scholar]
- 20.Bell R, Kingston J, Mogg T, Perkins N. The prevalence of gastric ulceration in racehorses in New Zealand. N Z Vet J. 2007;55:13–18. doi: 10.1080/00480169.2007.36729. [DOI] [PubMed] [Google Scholar]
- 21.Nadeau JA, Andrews FM, Mathew AG, et al. Evaluation of diet as a cause of gastric ulcers in horses. Am J Vet Res. 2000;61:784–790. doi: 10.2460/ajvr.2000.61.784. [DOI] [PubMed] [Google Scholar]
- 22.Lybbert T, Gibbs P, Cohen N, Scott B, Sigler D, Green E. Feeding alfalfa hay to exercising horses reduces the severity of gastric squamous mucosal ulceration. Proc 53rd Annu Conv Am Assoc Equine Pract; Orlando, Florida. 2007. pp. 525–526. [Google Scholar]
- 23.Mönki J, Hewetson M, Virtala AM. Risk factors for equine gastric glandular disease: A case-control study in a Finnish referral hospital population. J Vet Intern Med. 2016;30:1270–1275. doi: 10.1111/jvim.14370. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Sykes B, Jokisalo J. Rethinking equine gastric ulcer syndrome: Part 1–Terminology, clinical signs and diagnosis. Equine Vet Educ. 2014;26:543–547. [Google Scholar]
- 25.Peretich AL, Abbott LL, Andrews FM, Dhar MS. Age-dependent regulation of sodium-potassium adenosinetriphosphatase and sodium-hydrogen exchanger mRNAs in equine nonglandular mucosa. Am J Vet Res. 2009;70:1124–1128. doi: 10.2460/ajvr.70.9.1124. [DOI] [PubMed] [Google Scholar]
- 26.Cheng Y, Macera CA, Davis DR, Blair SN. Physical activity and peptic ulcers. Does physical activity reduce the risk of developing peptic ulcers? West J Med. 2000;173:101–107. doi: 10.1136/ewjm.173.2.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Snow D, Douglas T, Thompson H, Parkins J, Holmes P. Phenylbutazone toxicosis in equidae: A biochemical and pathophysiological study. Am J Vet Res. 1981;42:1754–1759. [PubMed] [Google Scholar]
- 28.MacKay R, French T, Nguyen H, Mayhew I. Effects of large doses of phenylbutazone administration to horses. Am J Vet Res. 1983;44:774–780. [PubMed] [Google Scholar]
- 29.Collins L, Tyler D. Phenylbutazone toxicosis in the horse: A clinical study. J Am Vet Med Assoc. 1984;184:699–703. [PubMed] [Google Scholar]
- 30.MacAllister C, Morgan S, Borne A, Pollet R. Comparison of adverse effects of phenylbutazone, flunixin meglumine, and ketoprofen in horses. J Am Vet Med Assoc. 1993;202:71–77. [PubMed] [Google Scholar]
- 31.Monreal L, Sabate D, Segura D, Mayós I, Homedes J. Lower gastric ulcerogenic effect of suxibuzone compared to phenylbutazone when administered orally to horses. Res Vet Sci. 2004;76:145–149. doi: 10.1016/j.rvsc.2003.10.004. [DOI] [PubMed] [Google Scholar]
- 32.Collins L, Tyler D. Experimentally induced phenylbutazone toxicosis in ponies: Description of the syndrome and its prevention with synthetic prostaglandin E2. Am J Vet Res. 1985;46:1605–1615. [PubMed] [Google Scholar]
- 33.Pedersen SK, Cribb AE, Read EK, French D, Banse HE. Phenylbutazone induces equine glandular gastric disease without decreasing prostaglandin E2 concentrations. J Vet Pharmacol Ther. 2018;41:239–245. doi: 10.1111/jvp.12464. [DOI] [PubMed] [Google Scholar]
- 34.D’Arcy-Moskwa E, Noble G, Weston L, Boston R, Raidal S. Effects of meloxicam and phenylbutazone on equine gastric mucosal permeability. J Vet Intern Med. 2012;26:1494–1499. doi: 10.1111/j.1939-1676.2012.01004.x. [DOI] [PubMed] [Google Scholar]
- 35.Covalesky M, Russoniello C, Malinowski K. Effects of show-jumping performance stress on plasma cortisol and lactate concentrations and heart rate and behavior in horses. J Equine Vet Sci. 1992;12:244–251. [Google Scholar]
- 36.Cayado P, Muñoz-Escassi B, Dominguez C, et al. Hormone response to training and competition in athletic horses. Equine Vet J. 2006;38:274–278. doi: 10.1111/j.2042-3306.2006.tb05552.x. [DOI] [PubMed] [Google Scholar]
- 37.Levenstein S, Rosenstock S, Jacobsen RK, Jorgensen T. Psychological stress increases risk for peptic ulcer, regardless of Helicobacter pylori infection or use of nonsteroidal anti-inflammatory drugs. Clin Gastroenterol Hepatol. 2015;13:498–506. doi: 10.1016/j.cgh.2014.07.052. [DOI] [PubMed] [Google Scholar]
- 38.Deding U, Ejlskov L, Grabas MPK, Nielsen BJ, Torp-Pedersen C, Bøggild H. Perceived stress as a risk factor for peptic ulcers: A register-based cohort study. BMC Gastroenterol. 2016;16:140. doi: 10.1186/s12876-016-0554-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Habershon-Butcher J, Hallowell G, Bowen I, Sykes B. Prevalence and risk factors for ulceration of the gastric glandular mucosa in Thoroughbred racehorses in training in the UK and Australia. J Vet Intern Med. 2012;26:731–731. [Google Scholar]