Rethinking equine gastric ulcer syndrome: Part 3 – Equine glandular gastric ulcer syndrome (EGGUS)

It has recently been highlighted that significant differences exist between ulceration of the squamous gastric mucosa and ulceration of the glandular gastric mucosa in the horse. The first article in this series discussed terminology, clinical signs and diagnosis and the second reviewed ulceration of the squamous gastric mucosa in detail. The purpose of this article, the third and last in the series, is to review the pathophysiology, risk factors, prevalence, treatment and prevention of ulceration of the glandular gastric mucosa.     

Rethinking equine gastric ulcer syndrome: Part 1 – Terminology,clinical signs and diagnosis

Equine gastric ulcer syndrome (EGUS) is a common condition in the horse. A series of recent articles highlighting differences in healing of squamous and glandular ulceration have reinvigorated interest in the condition. The purpose of this series of articles is to review the current thinking on EGUS with particular emphasis on the differences between diseases of the squamous and glandular mucosae. This article, the first will review the terminology, clinical signs and diagnosis of EGUS in the horse.     

The prevalence and distribution of gastric ulceration in 345 racehorses

OBJECTIVE: To report the prevalence and distribution of gastric ulceration within a group of racehorses and to describe the endoscopic appearance of gastric antrum and pyloric ulceration. DESIGN: Retrospective clinical study. PROCEDURE: Medical records from gastroscopic examinations of 345 racehorses (331 Thoroughbreds and 14 Standardbreds) were reviewed. Prevalence, distribution and severity of gastric ulcers were recorded. Lesions involving the squamous mucosa and the glandular mucosa of the antrum and pylorus were graded and compared. RESULTS: Gastric ulceration was found in 86% of racehorses. The squamous mucosa around the margo plicatus was most commonly affected. The pylorus was examined in 175 horses and 47% were ulcerated. No association was found between presence of lesions of the squamous mucosa and those of the pylorus. Low correlation was found between grade and location of lesions, with the pyloric lesion score being significantly less than the squamous mucosal lesion score. CONCLUSION: Gastric ulceration was present in a large proportion of racehorses. The pylorus was also an important site of ulceration. There was no association between presence of lesion at one site and the other, although there was a low correlation between grade of lesion and location, with the pyloric ulcer grade being lower.     

Effects of short-term light to heavy exercise on gastric ulcer development in horses and efficacy of omeprazole paste in preventing gastric ulceration

OBJECTIVE: To determine the effects of 8 days of light to heavy exercise on gastric ulcer development in horses and determine the efficacy of omeprazole paste in preventing gastric ulceration. DESIGN: Randomized, controlled, multicenter clinical trial. ANIMALS: 102 horses with normal-appearing gastric mucosa on endoscopic examination that were in light to heavy training. PROCEDURES: Horses at 4 trial locations were allocated into replicates and sham dosed orally (empty syringe) or treated with a paste formulation of omeprazole (1 mg/kg [0.45 mg/ lb], PO) once daily for 8 days. Training regimens varied among locations and included early training for western performance events; walking, trotting, and cantering in a mechanical exerciser; and race training (2 locations). Prevalences of gastric ulceration at the completion of the 8-day treatment period were compared between groups. RESULTS: At the end of the 8-day treatment period, the proportion of omeprazole-treated horses free from gastric ulceration (88%) was significantly higher than the proportion of sham-dosed horses free from gastric ulceration (27%). CONCLUSIONS AND CLINICAL RELEVANCE: Results showed that horses in light to heavy training for as short as 8 days were at risk of developing gastric ulcers and that administration of omeprazole paste decreased the incidence of gastric ulcers.     

Comparative endoscopic evaluation of normal and ulcerated gastric mucosae in Thoroughbred foals

To contribute to early diagnosis and treatment of gastric ulcer of foals, we examined the gastric mucosa of healthy and affected foals using an endoscope. In healthy foals, the characteristic changes in the development of the squamous mucosa were seen mainly in the squamous mucosa, and maturation of the squamous mucosa in the greater curvature (GC-S) occurred more slowly than that of the squamous mucosa in the lesser curvature (LC-S). Epithelial desquamation in the LC-S and GC-S was observed between 6 and 90 days but was not observed in the LC-S at about 60 days, whereas it was observed in the GC-S until 90 days old. These findings suggest that there is a difference in the development of the gastric mucosa by region and that desquamation continues over a term longer than studies have reported in the past. In the affected foals, the minimum age at which gastric ulcer was observed was 4 days old. Gastric ulcers formed predominantly in the squamous mucosa (LC-S and GC-S) of foals with an immature mucosa before the weaning period, and the peak incidence occurred between 61 and 90 days old. The differences in the ulceration sites were considered to depend on the difference in the development (maturation) stage of the squamous mucosa. The grading score of the gastric ulcer increased with the growth of the affected foals. The gastric ulcer might be enhanced greatly by stress in the weaning period.     

Equine gastric ulcer syndrome in adult horses: a review

In recent years, gastric ulceration has been recognised as a common, possibly performance-limiting disease of adult horses. Here, we aim to provide the reader with a useful review of recent literature covering all aspects of equine gastric ulcer syndrome (EGUS) in adult horses. The anatomy and physiology of the stomach, with particular reference to secretion of acid and mucosal protective mechanisms, are reviewed, as are the differing theories relating to the aetiopathogenesis of gastric ulceration. We also explore the possible influence of various management factors on development of the disease. The prevalence of the disease in racehorses has been reported to be as high as 100%. In general, horses that are in active training for racing tend to have a prevalence of around 90%, whereas pleasure horses in full work have a reported prevalence of approximately 60%. Emerging diagnostic tests which could obviate the need for gastroscopy are introduced and current recommendations for treatment are summarised, focussing on proton pump inhibitors, in particular omeprazole, administered orally. The oral administration of omeprazole has been shown to be effective in both treating horses with gastric ulceration and at preventing re-occurrence whilst the horses are in training, provided that daily dosing is maintained.     

Prevalence of gastric ulcers in endurance horses--a preliminary report

Gastric endoscopy was performed at the end of a 50 or 80 km endurance ride. Gastric ulceration was evident in 67% of the horses with ulcers on the squamous region of the stomach found in 57% of the horses and active bleeding of the glandular mucosa in 27%. Three horses (10%) had lesions only on the glandular mucosa. Values of albumin, creatinine and glucose were higher in horses without gastric lesions. We conclude that horses from endurance competitions have a high prevalence of gastric ulceration that is similar to that observed in performance horses. However the severity of ulceration is less severe than has been reported in Thoroughbred race horses in active training. Owners should be aware of the high prevalence of gastric ulceration in horses that perform in endurance competitions. The high incidence of active bleeding from the glandular mucosa of the stomach in these horses requires further investigation.     

Courses for horses: Rethinking the use of proton pump inhibitors in the treatment of equine gastric ulcer syndrome

Oral omeprazole has been the cornerstone of equine gastric ulcer syndrome (EGUS) treatment for nearly 20 years. However, approximately 15–30% of equine squamous gastric disease (ESGD) cases and 75% of equine glandular gastric disease (EGGD) cases fail to heal within current treatment guidelines. Recently, a number of factors that may affect the efficacy of oral omeprazole have been highlighted and the pharmacodynamics of a number of novel proton pump inhibitors (PPIs) have been described in the horse. The purpose of this article is to review the factors that affect oral omeprazole efficacy, with the goal of maximising therapeutic response, and the novel PPIs recently described.     

Prevalence of gastric ulceration in Swedish Standardbreds in race training

REASONS FOR PERFORMING STUDY: There is little information about the prevalence of gastric ulcers in Standardbred trotters and potential correlations between ulcers and various traits, e.g. age, sex, performance, temperament and feeding regimens, need further elucidation. OBJECTIVES: The prevalence of ulcers in the gastric squamous mucosa of Swedish Standardbreds was estimated and the associations between ulcer score and age, sex, performance, temperament and feeding regimens were determined. METHODS: Eighty Swedish Standardbreds in active race training, trained by 9 different trainers, underwent gastroscopy. Information on age, gender, status of training, performance over the last 4 months compared with the trainer's expectations before that period, behaviour, eating habits, feed type, bedding type, time spent outdoors per day and medical treatment during the last month was collected. Gastroscopy was performed and lesions in the squamous gastric mucosa were scored from 0 to 4 (0 = no lesions; 4 = > 5 lesions with haemorrhage, > 10 lesions with no haemorrhage, or a large area of diffuse loss of surface epithelium). RESULTS: Twenty-four (30%) of the horses had no lesions in the squamous mucosa, 22 (27.5%) had a score of 1; 21 (26.2%) score 2; 9 (11.2%) score 3; and 4 (5%) score 4. Horses that were in preparatory training and those that had raced during the last month were significantly more affected than horses that were fit for racing but had not raced during the last month, using a logistic regression model with trainer incorporated as a random effect. CONCLUSIONS: The study confirmed a high prevalence of ulcers in the gastric squamous mucosa of Standardbreds in race training. Of the studied parameters only status of training showed a significant association with gastric ulcers of the squamous mucosa. POTENTIAL RELEVANCE: Gastric ulceration is a common disease and diagnosis should be made by endoscopic examination of the gastric mucosa, since parameters such as age, gender, performance, behaviour, eating habits provide only weak clues as to which horses might be affected. Further studies are needed to determine the aetiology of the syndrome and to find ways to reduce, if possible, the frequency of gastric ulcers.     

Squamous gastric ulceration complicated by gastric stenosis in a foal

A 2-month-old Warmblood colt presented with recurrent colic and regurgitation. Gastroscopy, performed on several occasions, and barium-contrast radiography revealed severe squamous gastric ulceration and stenosis at the level of the margo plicatus. Treatment with omeprazole reduced the extent and severity of the gastric ulcers but did not affect the stenosis. The foal was euthanised because of a poor prognosis, and post-mortem examination confirmed the clinical diagnosis. Severe squamous gastric ulceration, granulation tissue formation and cicatrisation of deep gastric lesions were considered to have caused the stenosis. Gastroduodenal outflow obstruction is a recognised disorder in foals, but stenosis at the level of the margo plicatus has not been reported in foals or adult horses. To the authors' knowledge, this is the first case of severe squamous gastric ulceration, complicated by stenosis at the level of the margo plicatus, in a foal. Although rare, gastric stenosis should be considered in foals suffering recurrent colic and regurgitation.     

Associations between age or sex and prevalence of gastric ulceration in Standardbred racehorses in training

OBJECTIVE: To determine associations between age, sex, or medical treatment and prevalence and severity of gastric ulceration in Standardbred racehorses in training. DESIGN: Cross-sectional study. ANIMALS: 224 Standardbred racehorses in training. PROCEDURE: Gastroscopy was performed on each horse, and mucosal ulceration was graded from 0 (normal mucosa, no lesions) to 3 (extensive, often coalescing, lesions with areas of deep ulceration). Associations between age, sex, or treatment and prevalence and severity of ulcers were evaluated. RESULTS: Prevalence of gastric ulceration was 87%. Although there was little association between age and prevalence of ulcers, there was an association between age and severity of ulcers. Most 2-year-old horses (57.7%) had an ulcer score of 0 or 1. In all other age groups, most (58% to 82.61%) of horses had an ulcer score of 2 or 3. Although overall prevalence of ulceration was comparable among sex groups, the relative risk for gastric ulceration increased with age in castrated males, whereas it decreased in females and sexually intact males. CONCLUSIONS AND CLINICAL RELEVANCE: Gastric ulceration is common in Standardbred horses in race training. Severity is higher in horses > or = 3 years of age than in 2-year-old horses. Relative risk for ulceration increases with age in castrated males.     

Perforated gastric ulcer v associated with pyloroplasty for chronic hypertrophic pyloric gastropathy in a dog

A six-year-old male silkie terrier presented with a history of chronic vomiting. A diagnosis of gastric outflow obstruction was made using contrast radiography of the upper gastrointestinal tract. Surgical examination of the stomach revealed thickened pyloric antral mucosa. A Heineke-Mikulicz pyloroplasty combined with resection of the hypertrophic pyloric mucosa were performed to increase the patency of the pyloric lumen. The dog recovered well from surgery and his condition remained stable until the sixth day postoperatively when his condition deteriorated rapidly resulting in his death that night. At autopsy a perforated gastric ulcer was found in the cardiac region of the pylorus with evidence for a generalised peritonitis. An association between gastric outflow obstruction and gastric ulceration has been reported in human clinical literature and in canine experimental models. No such association has been previously documented in the veterinary clinical literature.     

Porcine gastric ulcer.

Ulceration of the pars esophagea in swine develops from a complex interaction of dietary particle size, gastric fluidity, dietary carbohydrate content, and presence of certain species of commensal gastric organisms capable of fermenting dietary carbohydrates. Unlike in humans, the significance of the role of Helicobacter sp. in development of porcine gastric ulcers is yet undefined. Management practices that limit the incidence and severity of gastric ulceration without interfering with growth performance appear to be the best option for control.     

Prevalence of gastric ulcers in show horses.

OBJECTIVE: To determine prevalence and risk factors for gastric ulcers in show horses. DESIGN: Field survey. ANIMALS: 50 horses in active training that had been transported to at least 1 event in the 30 days prior to endoscopy. PROCEDURE: Interview of owner, physical examination, serum biochemical analysis, CBC, and gastric endoscopy were performed. RESULTS: Gastric ulceration was detected in 58% of the horses. Horses with a nervous disposition were more likely to have ulceration than quiet or behaviorally normal horses. Horses with gastric ulceration had significantly lower RBC counts and hemoglobin concentrations than those without ulceration. CONCLUSIONS AND CLINICAL RELEVANCE: Show horses have a high prevalence of gastric ulceration. Lower RBC counts and hemoglobin concentrations may be the result of chronic gastric ulceration.     

A study of gastric mucosal pH and its correlation with gastric ulcers in adult horses

In a sample of twenty adult horses' stomachs, the mucosal surface pH was measured at 14 different loci, immediately post mortem, using a pH probe. The squamous epithelium of the pars oesophagea was observed to show a lower pH than the glandular mucosa. The pH of the glandular mucosa was generally uniform whereas within the pars oesophagea the different loci were observed to show variation, the lowest readings being found where the squamous epithelium adjoins the margo plicatus, the same area where ulceration initially tends to occur.

Ten horses in the sample showed moderate to severe ulceration and these horses had significantly lower pH readings compared to the group with mild to no ulceration.     

A comparison of the prevalence of gastric ulceration in feral and domesticated horses in the UK

Equine gastric ulcer syndrome is common in domesticated horses, especially those performing in athletic endeavours. However, the prevalence of equine gastric ulcer syndrome in feral populations of horses is not documented. This study investigated the prevalence and severity of squamous and glandular gastric ulceration in an abattoir population of horses in the UK. Both squamous and glandular ulceration were more prevalent in domesticated horses when compared to the feral horses studied.     

Endoscopic findings of the gastric antrum and pylorus in horses: 162 cases (1996-2000)

Medical records and endoscopy images were examined for 209 horses that had gastroscopic examinations performed with a 2.5- or 3-m-long endoscope by one of the authors (MJM) during a 4-year period (1996-2000). The antrum and pylorus were viewed in 162 horses, and the duodenum was viewed in 94 horses. Of these 162 horses, the gastric squamous mucosa was seen in 157 horses and 50% or more of the glandular mucosa of the body of the stomach was seen in 156 horses. Erosions or ulcers were seen in the gastric squamous mucosa in 91 (58%) horses. Erosions or ulcers were seen in the glandular mucosa of the body of the stomach in only 8% of the horses. Lesions consisting of erosion or ulceration were seen in the antrum or pylorus in 94 (58%) horses. Lesions consisting of hyperemia and a rough or "bumpy" appearance were seen in the mucosa of the duodenum of 16 horses. An association between the presence of lesions in the squamous mucosa and the presence of lesions in the mucosa of the antrum/pylorus was examined by Fisher's exact test, and the linear association of lesion severity scores between the squamous mucosa and the mucosa of the antrum/pylorus was tested using a Monte Carlo estimate for linear-by-linear association. There was no association (P = .88) between these sites for presence of lesions or lesion severity scores. Similarly, there was no association between scores for the glandular mucosa in the gastric body and those in the antrum/pylorus. Because of the high prevalence of lesions in the antrum and pylorus of the stomachs of adult horses examined in a hospital setting, the entire stomach should be viewed during a gastroscopic examination.     

Effects of treatment with omeprazole or ranitidine on gastric squamous ulceration in racing Thoroughbreds

OBJECTIVE: To compare the effects of oral administration of omeprazole and ranitidine on gastric squamous ulceration in Thoroughbreds in race training. DESIGN: Modified crossover study. ANIMALS: 60 Thoroughbreds in race training with gastric squamous mucosal ulceration. PROCEDURE: Horses were randomly allocated into 3 groups. Group 1 received no treatment for 28 days followed by administration of omeprazole (4 mg/kg [1.8 mg/lb], PO, once daily) for 28 days; group 2 received omeprazole (4 mg/kg, PO, once daily) for 28 days followed by no treatment for 28 days; and group 3 received ranitidine (6.6 mg/kg [3.0 mg/lb], PO, q 8 h) for 28 days followed by administration of omeprazole (4 mg/kg, PO, once daily) for 28 days. Ulceration was assessed endoscopically at days 0, 28, 42, and 56. Lesions were scored from 0 (no ulceration) to 3 (severe ulceration). RESULTS: After the initial 28 days of treatment, the decrease in ulcer severity was significantly greater after omeprazole treatment than after ranitidine treatment. Ulcer severity decreased significantly in group 3 horses after 14 days of treatment with omeprazole. Discontinuation of omeprazole resulted in worsening of ulcer scores; however, ulcer scores at completion of the study were less than at day 0. Horses that received omeprazole after 28 days of ranitidine treatment had a further reduction in ulcer severity. CONCLUSIONS AND CLINICAL RELEVANCE: Omeprazole was more effective than ranitidine in healing gastric squamous ulcers in Thoroughbreds in race training. Improvement was detected by 14 days and persisted in most of the group 2 horses for at least 28 days after omeprazole treatment was discontinued.     

The effect of a pectin-lecithin complex on prevention of gastric mucosal lesions induced by feed deprivation in ponies

This study examined whether a product containing a pectinlecithin complex (Pronutrin) (1) could prevent gastric lesions induced in the equine gastric squamous epithelial mucosa using a protocol of intermittent feed deprivation that resulted in prolonged increased gastric acidity (Murray and Eichorn 1996). Eight ponies were used and served as their own controls in 2 trials in which there were 72 h cumulative deprivation (alternating 24 h with no feed, then 24 h free choice hay), with a 4-week interval between trials. Ponies were assigned randomly to receive either 250 g Pronutrin plus 200 g pelleted feed, or 450 g pelleted feed only. Ponies were conditioned to each treatment for 7 days and received Pronutrin and pellets or only pellets once daily during the feed deprivation protocol. Gastroscopy was performed at the beginning and conclusion of the feed deprivation protocol. The endoscopist (MJ.M.) was blinded as to treatments, and lesion severity was scored on a scale of 0-5. Gastroscopy revealed normal-appearing gastric mucosa at the beginning of feed deprivation, with the exception of 2 ponies which had focal squamous mucosal erosion and 1 pony with focal glandular mucosal erosion. After 72 h cumulative feed deprivation, each pony, except 1 pony in one of the trials, developed erosions or ulcers in the gastric squamous mucosa. There was no difference (P = 0.6) in the presence or severity of gastric lesions between treatments. Lesions did not develop in the gastric glandular mucosa as a result of the intermittent feed deprivation with either treatment. In this study, the pectin-lecithin complex in Pronutrin failed to prevent lesions in the gastric squamous mucosa induced by intermittent feed deprivation.     

Prevalence of gastric ulcer syndrome in high-level endurance horses

Reasons for performing the study: Equine gastric ulcers syndrome (EGUS) prevalence studies are rare in the endurance horse and none has been carried out to date in horses competing at high level. Objectives: To determine the prevalence of EGUS in high‐level endurance horses. Methods: Thirty endurance horses competing at high level were selected and submitted to 2 gastroscopic examinations. The first gastroscopy was performed during the interseason period, and the second during the competition season within 2–3 days following a ride of 90–160 km. Data related to housing, feeding, training system as well as age, breed and gender were recorded for each horse. Results: The prevalence of squamous gastric ulcers was 48% during the interseason period (mean score 0.85 ± 0.13 on a scale from 0–4) and 93% during the competition season (mean score 1.60 ± 1.15) with a highly significant difference between the seasons (P = 0.001). Most of the lesions were situated in the squamous portion of the stomach but 33.3% of horses showed also glandular lesions. Significant influence of training and performance level on the gastric score (according to the distance of the ride preceding the second gastroscopy) was shown (P = 0.038). There was also a significant influence of housing on the gastric score (P = 0.002) showing higher scores in the horses kept totally on pasture (mean score: 2.14 ± 0.14) vs. horses housed in a mixed environment (stable + pasture, mean score: 1.43 ± 0.17). Both the pastured and (stabled + pastured) groups were receiving a grain supplement but the pastured group received a higher daily starch intake, which might explain the higher ulcer prevalence. There was no influence of age, breed or gender on the gastric scores. Conclusions: The high prevalence of gastric lesions observed in this study is probably related to the high level of training and performance of the horses examined compared to the population of horses included in the prior study. Potential relevance: This prevalence of EGUS in high‐level endurance horses is comparable to the prevalence established in racing horses. The equine veterinarians may take into consideration EGUS as a potential cause of poor performance.