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Prevalence of non-glandular gastric ulcers in horses involved in a university riding program
Scientific Papers Prevalence of Non-Glandular Gastric Ulcers in Horses Involved in a University Riding Program Kelly A. Chameroy, MS,a Jenifer A. Nadeau, MS, PhD,a* Sandra L. Bushmich, MS, DVM,b James E. Dinger, PhD,a Thomas A. Hoagland, PhDa, and Arnold M. Saxton, PhDc
ABSTRACT The objective of the study was to determine the prevalence of gastric ulcers in horses involved in a university riding program. Researchers examined 80 riding horses engaged in hunt seat lessons, stock seat lessons, polo, and training (breeds included Morgans, Quarter Horses including crosses, Thoroughbreds, and other lineage). Gastroscopic examination was performed to determine the presence of gastric ulcers. Non-glandular ulcers present were scored using an accepted scoring system. Descriptive characteristics such as age, sex, breed, housing, use, and prior medication of horses were recorded. Nine (11%) of the horses had non-glandular ulcerations. Age and sex had a significant (P < .05) effect on non-glandular ulcers in this population. Horses that were 2 to 6 or 18 to 23 years of age and mares were most affected by non-glandular gastric ulcers. Non-glandular ulcer occurrence was lower in this population than in any previous studies focused on elite, heavy-use performance horses, show horses, racehorses, and recreational horses. Horses used predominantly in their home environment may suffer from a lower occurrence of non-glandular gastric ulcers than previously studied populations such as racing and show horses despite the frequency and intensity of their activities.
INTRODUCTION Previous studies have found non-glandular gastric ulcers to be a significant problem in horses engaged in strenuous exercise or training such as racing Thoroughbreds, competition, endurance, and show horses.1-7 In these studies, prevalence of non-glandular gastric ulcers was found to range from 37% to 93%. Other studies suggested that frequent traveling over long distances, frequent work, and the many environmental and dietary changes related to showing may have a negative influence on the ability of the non-glandular gastric mucosa to withstand damage.5,7 Studies have not examined horses mainly used in their home environment and rarely shown, such as horses used in a university program and riding school horses. This study challenges the previously held assumption that recreational riding horses may have a high incidence of nonglandular gastric ulceration. The purpose of the study was to determine the prevalence of gastric ulcers in 80 university-owned and housed horses used for hunt seat lessons, stock seat lessons, polo, and training and the effects of age, breed, sex, housing, and use on the affected horses.
Key words: non-glandular ulcer; ulcer prevalence; age; sex
A total of 80 horses of varying uses, breeds, ages, and sexes participated in the study. Horses were part of a university equine program (owned and housed at the university) and were used for polo, hunt seat lessons, stock seat lessons, or training. Breed groups were defined as Morgans, Quarter Horses (including crosses), Thoroughbreds, or other. The horses used in this study ranged in age from 2 to 23 years. Twenty-eight horses were 2 to 6 years old, 34 horses were 8 to 17 years old, and 18 horses were 18 to 23 years old. There were 32 Thoroughbreds, 24 Morgans, 6 Quarter Horses includ-
From the Departments of aAnimal Science and bPathobiology and Veterinary Science, University of Connecticut, Storrs, Connecticut; and the cDepartment of Animal Science, University of Tennessee, Knoxville, Tennessee. Reprint requests: Jenifer A. Nadeau, University of Connecticut, 3636 Horsebarn Rd. Ext. U-4040, Storrs, CT 06269-4040 0737-0806/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.jevs.2006.03.001
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MATERIALS AND METHODS
Selection of Horses
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ing crosses, and 18 other breeds of horses in the study. Forty-nine were geldings, and 31 were mares. Twenty-six hunt and stock seat lesson horses, 31 polo horses, and 23 horses in training for hunt and stock seat lesson were used in the study. Horses were either housed in stalls with turnout time (lesson horses), stalls without consistent turnout time (polo horses), or outside with run-in sheds (horses in training). All horses were fed a diet of orchard grass hay (6.5 kg/day) and a 14% protein concentrate (10 lb/day/horse). All animals were routinely dewormed every 6 to 8 weeks. Horse health histories, including animal’s sex, age, breed, previous medical problems, and use, were gathered. Ninety-five horses were present on the farm, but only eighty horses were scoped. The horses not chosen for gastroscopy were breeding stock, animals younger than 2 years of age, those having nasal passages too narrow to allow passage of the endoscope, and those found to have a health problem during the pre-procedure examination (such as cardiac arrhythmia). Of the 80 horses scoped, only one was documented as having received a nonsteroidal anti-inflammatory drug (NSAID) (flunixin meglumine, 400 mg, intravenously) within 2 months before endoscopy for mild colic. None of the horses studied had received any type of acid-suppressive treatments either within 2 months of being scoped, or, in the case of newly acquired horses, at any time since being owned by the university.
Endoscopic Gastroscopy The following protocol was approved by the University of Connecticut Animal Care and Use Committee. Animals that were to be scoped were placed in box stalls with pine bedding. The night before endoscopy, feed and manure was removed at 8:00 pm. Feed was withheld until 1 hour post-endoscopy. Horses were allowed access to water until about 2 hours before endoscopy. The total amount of time without feed ranged from 14 to 16 hours, and water from 2 to 4 hours, to allow for adequate emptying of the stomach. Horses were confined in breeding stocks fixed in concrete and sedated using one of two drug combinations. Combination 1 consisted of xylazine (0.66 mg/kg, IV) and acepromazine (0.033 mg/kg, IV). In combination 1, both drugs were administered at the same time, 10 minutes before endoscopy. Combination 2 consisted of detomidine (0.11 mg/kg, IV), butorphanol (0.0066 mg/kg, IV), and acepromazine (0.033 mg/kg, IV). In combination 2, acepromazine was given 10 minutes before endoscopy, whereas the other two drugs were administered on placement of the horse in the stocks 5
208
minutes before endoscopy. The decision on which combination to use was determined based on the horse’s age and temperament. Horses from 2 to 4 years of age were given combination 2, as well as those that were excitable or nervous, to decrease risk of injury to animal and handler. A nasal twitch was applied for further restraint. Body weight was determined using a livestock scale or a standard weight tape. Images were recorded onto standard VHS videocassettes using a VCR connected to a 3.4-m long video endoscope (Xion Medical, Berlin, Germany). The endoscope was covered with a water-based lubricating gel to ease passage. On passing through the cardiac sphincter into the antrum of the stomach, the stomach was insufflated with air and the endoscope was directed toward the margo plicatus. Views were obtained along the margo plicatus of both the glandular and non-glandular regions. After endoscopy, horses were returned to their stalls and observed for 1 hour. After 1 hour, horses were given hay and water.
Scoring Ulcers were scored using an accepted gastric ulcer scoring system.8 Two scores were obtained for each horse. The first score was for the number of non-glandular lesions observed, defined as follows: 0 (no lesions), 1 (1-2 localized lesions), 2 (3-5 localized lesions), 3 (6-10 lesions), and 4 [>10 lesions or diffuse (or very large) lesions]. The second score was for the non-glandular lesion severity and ranged from 0 to 5, defined as: 0 (no lesions), 1 (appears superficial), 2 [deeper structures involved (lesion has greater depth than number 1)], 3 [multiple lesions and variable severity (1, 2, or 4)], 4 [same as number 2 and has active (hyperemic or darkened lesion crater] appearance, and 5 (deep structures involved, having an active appearance with active hemorrhage or adherent blood clot).
Statistical Analysis The influence of treatments (sex, age, use, and breed) on the occurrence of non-glandular gastric ulcers and non-glandular gastric ulcer severity was tested by analysis of ranks for the non-normally distributed data using the Mixed Procedure of SAS (SAS/STAT User’s Guide Version 9.0, SAS Institute, Cary, NC).b A model for a completely randomized design was used, with main effects of all four treatment variables. All possible interactions among treatment variables were found to be non-significant (P > .10) and so were dropped from the model to reduce statistical adjustments in the unbalanced data. Because of the unbalance in horse number
Journal of Equine Veterinary Science
May 2006
Table 1
Ulcer number and severity scores by use breed, age, and sex of horses Ulcer Number Score
Ulcer Severity Score
0
1
2
3
0
1
2
3
4
5
Use Lessons (n = 26) Polo (n = 31) Training (n = 23)
23 29 19
0 1 0
2 1 2
0 1 2
23 29 19
0 2 1
1 0 0
0 0 2
1 0 1
0 1 0
Breed Morgan (n = 24) Other (n = 18) Quarter Horse incl. crosses (n = 6) Thoroughbred (n = 32)
19 17 6 29
0 1 0 0
3 0 0 2
2 0 0 1
19 17 6 29
1 1 0 1
0 0 0 1
2 0 0 0
2 0 0 0
0 0 0 1
Age* 2-6 Years old (n = 28) 8-17 Years old (n = 34) 18-23 Years old (n = 18)
22 34 15
0 0 1
4 0 1
2 0 1
22 34 15
1 0 2
1 0 0
2 0 0
2 0 0
0 0 1
Sex* Geldings (n = 49) Mares (n = 31)
46 25
0 1
2 3
1 2
46 25
2 1
0 1
0 2
1 1
0 1
*P < .05.
and lack of significance, use was dropped from the model when estimating least square means for the other main effects. Least square means from the untransformed data are reported for interpretation. Statistical differences were defined at the 5% significance level. RESULTS The length of time that feed and water were withheld allowed adequate, if not complete, emptying of stomach contents in all 80 horses used. Some animals had fluid or gastric contents present that slightly obscured some of the ventral portion of the gastric glandular mucosa. However, in all horses, the entire squamous mucosal lining was visible as was the gastric glandular mucosa directly adjacent to the margo plicatus. No parasites were observed on examination. Nine of the 80 horses (11%) had ulcers in the nonglandular squamous epithelial mucosa with lesion number scores ranging from 0 to 3 and lesion severity scores ranging from 0 to 5 (Table 1). Some horses lacking ulcers showed signs of hyperkeratosis. Lesions identified by gastroscopic examinations were all located along the margo plicatus in the nonglandular region. Lesions were distributed in various patterns, mainly multifocal, but some were focal as well as diffuse or linear. Horses with more severe ulcerations tended to have a combination of focal or multifocal lesions along with hyperemia, erosion, and some bleeding.
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Horses with non-glandular ulcers were in two different age groups, three of the four breed groups, both sexes, and all three use categories (Table 1). The horse that had received a single 8-mL dose of an NSAID within 2 months before being examined had no lesions visible on examination. Horses new to the facility were not more likely to have non-glandular ulcers. No significant differences were discovered among use or the four breed categories in either non-glandular ulcer severity scores or non-glandular ulcer number. There was a numerical trend for mean non-glandular ulcer number and mean non-glandular ulcer severity to be highest in horses used for training (17.4%), followed by horses used in polo (9.6%) and horses used in lessons (7.7%), respectively. Occurrence of non-glandular ulcers and severity of non-glandular ulcers differed across categories of age and gender (P < .05). Although we showed significant differences in these risk factors, the results should be interpreted with caution because of the small number of horses with gastric ulcers. No nonglandular ulcers were observed among the 8- to 17year-olds, whereas non-glandular ulcers occurred within 2 to 6-year-olds (21.4%), and 18- to 23-yearolds (16.7%). Mean non-glandular ulcer number and mean non-glandular ulcer severity score was higher (P < .05) among the 2- to 6-year-olds when compared with 18- to 23-year-olds. Mean non-glandular ulcer
209
number and mean non-glandular ulcer severity score was higher (P < .05) among mares (19.3%) when compared with geldings (6.1%). DISCUSSION Others have reported that the most common location of gastric ulcers horses in training is within the squamous epithelial mucosa, with the most severe and greatest abundance of lesions occurring adjacent to the margo plicatus.5,9,10 All ulcerations in horses in this study were within the squamous epithelial mucosa adjacent to the margo plicatus. No glandular lesions were observed, however, the fluid or debris remaining in the stomachs of some of the animals, even after several hours of fasting, may have partially obscured our views of the glandular region. This study did not find a difference in the occurrence of non-glandular ulcers based on the breed of the horses studied. In a previous study, Thoroughbreds and Standardbreds were found to have a higher occurrence of gastric ulcers compared with Icelandic and Swedish Warmblooded horses.11 However, the number of affected horses in our study was much smaller, and making conclusions regarding the effect of breed is therefore difficult. The occurrence of ulcers among the three age groups was found to be significantly different, with no ulcers occurring in animals ranging in age from 8 to 17 years. A retrospective study of Swedish horses found that prevalence of gastric ulcerations decreased as animals aged.11 It has also been found that younger horses tend to be more susceptible to gastric ulcers.1,12,13 The results of this study appear to concur with the finding that gastric ulcers are common in young animals. Most non-glandular lesions occurred in the age group of 2- to 6-year-olds, primarily among the 3-year-olds. Three of the horses affected with non-glandular ulcers in our study population were 18 to 23 years old. The non-glandular ulcerations that occurred in the age group of 18to 23-year-olds occurred only in animals used in polo, which constituted 75% of this age group. Polo is an intense performance sport and exercise has been found to delay gastric emptying, subjecting the stomach to acid for a longer period, which may contribute to these horses’ susceptibility to gastric ulcers.2 A decrease in the amount of epidermal growth factor (EGF) produced by the salivary glands may lead to ulceration because it promotes cellular DNA synthesis and growth of the gastrointestinal mucosa.14 Again, with the small number of affected horses, whether this may also be true in the general population is difficult to say.
210
A difference in occurrence of ulcers between mares and geldings was found within the population. Sandin et al found that, among the sexes, stallions and mares had a greater occurrence of ulcers (18% and 12%, respectively) when compared with geldings (10%).11 In a study in Thoroughbred racehorses, more females were affected with ulcers than males.13 In reproductively intact animals (mares and stallions), there may be a hormonal influence on the tissues, affecting their resistance to damage, making the gastric tissue more prone to developing lesions. In the study reported here, 19% of the mares had non-glandular ulcers, whereas only 6% of the geldings had non-glandular ulcers. We did not find a difference in non-glandular ulcer occurrence depending on the use of horses in our study. A previous study found that increased intra-abdominal pressure during exercise pushes gastric contents into the non-glandular portion of the stomach.15 These researchers postulate that the reason non-glandular ulcers tend to develop or worsen when horses are in intensive training programs is the duration of exposure to these acidic contents. The horses in training in our study do not undergo intensive training regimens. They are not worked for extended periods at the gallop but rather train for a short time at the walk, trot, and canter, with most of the time spent walking and trotting. The polo horses in our study are low-goal polo horses and therefore also may spend less time galloping than other groups that have been previously studied. The riding horses used in our study are involved in basic hunt seat lessons with some jumping and also are not ridden intensively (ie, at faster gaits such as the gallop) for extended periods. This could explain why the horses in our study had a considerably lower prevalence than other working categories of horses that have been examined. The prevalence of non-glandular gastric ulcers was 11% for horses in this study. Other studies have found a much higher occurrence of non-glandular gastric ulcers than the study discussed here. A previous study found that horses not in race training and used for riding lessons, pleasure, or show had a 37% prevalence of gastric ulceration.2,9 A study of Standardbred racehorses found an 87% prevalence of gastric ulceration.12 The greatest occurrence of gastric ulcers was found in Thoroughbred racehorses, ranging from 66% to 93%.1,13 Perhaps the closest in similarity to our study population would be show horses, horses retired from racing, and Western performance horses. However, the occurrence of non-glandular gastric ulceration in these populations was much higher—58%, 52%, and 40%, respectively.1,5,6 The horses in our study did not travel to
Journal of Equine Veterinary Science
May 2006
shows or competitions, and were used in their home environment. Previous studies of show horses and horses in a simulated show or training environment suggested that frequent traveling over long distances, frequent work, and the many environmental and dietary changes related to showing may have a negative influence on the ability of the gastric mucosa to withstand damage.5,7 In this study, the lack of extensive use for showing and other activities that would result in increased transportation and dietary and environmental changes possibly contributed to the low occurrence of non-glandular ulcerations found. All of the horses except the polo horses had access to pasture for 6 months before the study and were used mainly for light to moderate work. The three polo horses that had gastric ulcers had not had access to pasture for 6 months before the study. A previous study found that horses having outdoor access and access to pasture had normal stomachs.16 The statistical analysis in this study is based on a small number of horses with gastric ulcers, so the validity of the data could be questioned. However, there were statistical differences based on age and sex that correspond to pre-existing data in the literature. The study results suggest that horses used predominantly in their own environment, despite the frequency and intensity of activity, may have a lower occurrence of nonglandular gastric ulcers than previously studied mobile populations such as racing and show horses.
REFERENCES 1. 2.
Hammond CJ, Mason DK, Watkins KL. Gastric ulceration in mature Thoroughbred horses. Equine Vet J 1986;18:284-287. Murray MJ, Grodinsky C, Anderson CW, Radue PF, Schmidt GR. Gastric ulcers in horses: a comparison of endoscopic findings in
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3.
4. 5. 6. 7. 8. 9. 10. 11.
12.
13. 14.
15. 16.
horses with and without clinical signs. Equine Vet J Suppl 1989;7:68-72. Vatistas NJ, Snyder JR, Carlson G, Johnson B, Arthur RM, Thurmond M, Lloyd KCK. Epidemiological study of gastric ulceration on the Thoroughbred racehorse: 202 horses 1992-1993. Proc 40th Annual Convention American Association Equine Practitioners 1994;125-126. 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. McClure SR, Glickman LT, Glickman NW. Prevalence of gastric ulcers in show horses. J Am Vet Med Assoc 1999;215:1130-1133. Bertone JJ. Prevalence of gastric ulcers in elite, heavy use western performance horses. Proc 46th Annual Convention American Association Equine Practitioners 2000;256-259. McClure SR, Carithers DS, Gross SJ, Murray MJ. Gastric ulcer development in horses in a simulated show or training environment. J Am Vet Med Assoc 2005; 227:775-777. MacAllister CG, Andrews FM, Deegan E, Ruoff W, Olovson SG. A scoring system for gastric ulcers in the horse. Equine Vet J 1997;29,430-433. Furr MO, Murray MJ. Treatment of gastric ulcers in horses with histamine type 2 receptor antagonists. Equine Vet J Suppl 1989;7:77-79. Murray MJ. Gastric ulcers in adult horses. The Compendium 1994;792-794,797. Sandin A, Skidell J, Häggström J, Girma K, Nilsson G. Postmortem findings of gastric ulcers in Swedish horses older than age one year: a retrospective study of 3715 horses (1924-1996). Equine Vet J 2000;32:36-42. 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. Murray MJ, Schusser GF, Pipers FS, Gross SJ. Factors associated with gastric lesions in Thoroughbred racehorses. Equine Vet J 1996;28:368-374. Gysin B, Muller RKM, Otten U, Fishlie AE. Epidermal growth factor content of submandibular glands is increased in rats with experimentally induced gastric lesions. Scand J Gastroenterol 1988;23:665-671. Lorenzo-Figueras M, Merritt AM. Effects of exercise on gastric volume and pH in the proximal portion of the stomach of horses. Am J Vet Res 2002;63:1481-1487. Murray MJ. Equine model of inducing ulceration in alimentary squamous epithelial mucosa. Dig Dis Sci 1994;39:2530-2535.
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ABSTRACT The objective of the study was to determine the prevalence of gastric ulcers in horses involved in a university riding program. Researchers examined 80 riding horses engaged in hunt seat lessons, stock seat lessons, polo, and training (breeds included Morgans, Quarter Horses including crosses, Thoroughbreds, and other lineage). Gastroscopic examination was performed to determine the presence of gastric ulcers. Non-glandular ulcers present were scored using an accepted scoring system. Descriptive characteristics such as age, sex, breed, housing, use, and prior medication of horses were recorded. Nine (11%) of the horses had non-glandular ulcerations. Age and sex had a significant (P < .05) effect on non-glandular ulcers in this population. Horses that were 2 to 6 or 18 to 23 years of age and mares were most affected by non-glandular gastric ulcers. Non-glandular ulcer occurrence was lower in this population than in any previous studies focused on elite, heavy-use performance horses, show horses, racehorses, and recreational horses. Horses used predominantly in their home environment may suffer from a lower occurrence of non-glandular gastric ulcers than previously studied populations such as racing and show horses despite the frequency and intensity of their activities.
INTRODUCTION Previous studies have found non-glandular gastric ulcers to be a significant problem in horses engaged in strenuous exercise or training such as racing Thoroughbreds, competition, endurance, and show horses.1-7 In these studies, prevalence of non-glandular gastric ulcers was found to range from 37% to 93%. Other studies suggested that frequent traveling over long distances, frequent work, and the many environmental and dietary changes related to showing may have a negative influence on the ability of the non-glandular gastric mucosa to withstand damage.5,7 Studies have not examined horses mainly used in their home environment and rarely shown, such as horses used in a university program and riding school horses. This study challenges the previously held assumption that recreational riding horses may have a high incidence of nonglandular gastric ulceration. The purpose of the study was to determine the prevalence of gastric ulcers in 80 university-owned and housed horses used for hunt seat lessons, stock seat lessons, polo, and training and the effects of age, breed, sex, housing, and use on the affected horses.
Key words: non-glandular ulcer; ulcer prevalence; age; sex
A total of 80 horses of varying uses, breeds, ages, and sexes participated in the study. Horses were part of a university equine program (owned and housed at the university) and were used for polo, hunt seat lessons, stock seat lessons, or training. Breed groups were defined as Morgans, Quarter Horses (including crosses), Thoroughbreds, or other. The horses used in this study ranged in age from 2 to 23 years. Twenty-eight horses were 2 to 6 years old, 34 horses were 8 to 17 years old, and 18 horses were 18 to 23 years old. There were 32 Thoroughbreds, 24 Morgans, 6 Quarter Horses includ-
From the Departments of aAnimal Science and bPathobiology and Veterinary Science, University of Connecticut, Storrs, Connecticut; and the cDepartment of Animal Science, University of Tennessee, Knoxville, Tennessee. Reprint requests: Jenifer A. Nadeau, University of Connecticut, 3636 Horsebarn Rd. Ext. U-4040, Storrs, CT 06269-4040 0737-0806/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.jevs.2006.03.001
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MATERIALS AND METHODS
Selection of Horses
207
ing crosses, and 18 other breeds of horses in the study. Forty-nine were geldings, and 31 were mares. Twenty-six hunt and stock seat lesson horses, 31 polo horses, and 23 horses in training for hunt and stock seat lesson were used in the study. Horses were either housed in stalls with turnout time (lesson horses), stalls without consistent turnout time (polo horses), or outside with run-in sheds (horses in training). All horses were fed a diet of orchard grass hay (6.5 kg/day) and a 14% protein concentrate (10 lb/day/horse). All animals were routinely dewormed every 6 to 8 weeks. Horse health histories, including animal’s sex, age, breed, previous medical problems, and use, were gathered. Ninety-five horses were present on the farm, but only eighty horses were scoped. The horses not chosen for gastroscopy were breeding stock, animals younger than 2 years of age, those having nasal passages too narrow to allow passage of the endoscope, and those found to have a health problem during the pre-procedure examination (such as cardiac arrhythmia). Of the 80 horses scoped, only one was documented as having received a nonsteroidal anti-inflammatory drug (NSAID) (flunixin meglumine, 400 mg, intravenously) within 2 months before endoscopy for mild colic. None of the horses studied had received any type of acid-suppressive treatments either within 2 months of being scoped, or, in the case of newly acquired horses, at any time since being owned by the university.
Endoscopic Gastroscopy The following protocol was approved by the University of Connecticut Animal Care and Use Committee. Animals that were to be scoped were placed in box stalls with pine bedding. The night before endoscopy, feed and manure was removed at 8:00 pm. Feed was withheld until 1 hour post-endoscopy. Horses were allowed access to water until about 2 hours before endoscopy. The total amount of time without feed ranged from 14 to 16 hours, and water from 2 to 4 hours, to allow for adequate emptying of the stomach. Horses were confined in breeding stocks fixed in concrete and sedated using one of two drug combinations. Combination 1 consisted of xylazine (0.66 mg/kg, IV) and acepromazine (0.033 mg/kg, IV). In combination 1, both drugs were administered at the same time, 10 minutes before endoscopy. Combination 2 consisted of detomidine (0.11 mg/kg, IV), butorphanol (0.0066 mg/kg, IV), and acepromazine (0.033 mg/kg, IV). In combination 2, acepromazine was given 10 minutes before endoscopy, whereas the other two drugs were administered on placement of the horse in the stocks 5
208
minutes before endoscopy. The decision on which combination to use was determined based on the horse’s age and temperament. Horses from 2 to 4 years of age were given combination 2, as well as those that were excitable or nervous, to decrease risk of injury to animal and handler. A nasal twitch was applied for further restraint. Body weight was determined using a livestock scale or a standard weight tape. Images were recorded onto standard VHS videocassettes using a VCR connected to a 3.4-m long video endoscope (Xion Medical, Berlin, Germany). The endoscope was covered with a water-based lubricating gel to ease passage. On passing through the cardiac sphincter into the antrum of the stomach, the stomach was insufflated with air and the endoscope was directed toward the margo plicatus. Views were obtained along the margo plicatus of both the glandular and non-glandular regions. After endoscopy, horses were returned to their stalls and observed for 1 hour. After 1 hour, horses were given hay and water.
Scoring Ulcers were scored using an accepted gastric ulcer scoring system.8 Two scores were obtained for each horse. The first score was for the number of non-glandular lesions observed, defined as follows: 0 (no lesions), 1 (1-2 localized lesions), 2 (3-5 localized lesions), 3 (6-10 lesions), and 4 [>10 lesions or diffuse (or very large) lesions]. The second score was for the non-glandular lesion severity and ranged from 0 to 5, defined as: 0 (no lesions), 1 (appears superficial), 2 [deeper structures involved (lesion has greater depth than number 1)], 3 [multiple lesions and variable severity (1, 2, or 4)], 4 [same as number 2 and has active (hyperemic or darkened lesion crater] appearance, and 5 (deep structures involved, having an active appearance with active hemorrhage or adherent blood clot).
Statistical Analysis The influence of treatments (sex, age, use, and breed) on the occurrence of non-glandular gastric ulcers and non-glandular gastric ulcer severity was tested by analysis of ranks for the non-normally distributed data using the Mixed Procedure of SAS (SAS/STAT User’s Guide Version 9.0, SAS Institute, Cary, NC).b A model for a completely randomized design was used, with main effects of all four treatment variables. All possible interactions among treatment variables were found to be non-significant (P > .10) and so were dropped from the model to reduce statistical adjustments in the unbalanced data. Because of the unbalance in horse number
Journal of Equine Veterinary Science
May 2006
Table 1
Ulcer number and severity scores by use breed, age, and sex of horses Ulcer Number Score
Ulcer Severity Score
0
1
2
3
0
1
2
3
4
5
Use Lessons (n = 26) Polo (n = 31) Training (n = 23)
23 29 19
0 1 0
2 1 2
0 1 2
23 29 19
0 2 1
1 0 0
0 0 2
1 0 1
0 1 0
Breed Morgan (n = 24) Other (n = 18) Quarter Horse incl. crosses (n = 6) Thoroughbred (n = 32)
19 17 6 29
0 1 0 0
3 0 0 2
2 0 0 1
19 17 6 29
1 1 0 1
0 0 0 1
2 0 0 0
2 0 0 0
0 0 0 1
Age* 2-6 Years old (n = 28) 8-17 Years old (n = 34) 18-23 Years old (n = 18)
22 34 15
0 0 1
4 0 1
2 0 1
22 34 15
1 0 2
1 0 0
2 0 0
2 0 0
0 0 1
Sex* Geldings (n = 49) Mares (n = 31)
46 25
0 1
2 3
1 2
46 25
2 1
0 1
0 2
1 1
0 1
*P < .05.
and lack of significance, use was dropped from the model when estimating least square means for the other main effects. Least square means from the untransformed data are reported for interpretation. Statistical differences were defined at the 5% significance level. RESULTS The length of time that feed and water were withheld allowed adequate, if not complete, emptying of stomach contents in all 80 horses used. Some animals had fluid or gastric contents present that slightly obscured some of the ventral portion of the gastric glandular mucosa. However, in all horses, the entire squamous mucosal lining was visible as was the gastric glandular mucosa directly adjacent to the margo plicatus. No parasites were observed on examination. Nine of the 80 horses (11%) had ulcers in the nonglandular squamous epithelial mucosa with lesion number scores ranging from 0 to 3 and lesion severity scores ranging from 0 to 5 (Table 1). Some horses lacking ulcers showed signs of hyperkeratosis. Lesions identified by gastroscopic examinations were all located along the margo plicatus in the nonglandular region. Lesions were distributed in various patterns, mainly multifocal, but some were focal as well as diffuse or linear. Horses with more severe ulcerations tended to have a combination of focal or multifocal lesions along with hyperemia, erosion, and some bleeding.
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Horses with non-glandular ulcers were in two different age groups, three of the four breed groups, both sexes, and all three use categories (Table 1). The horse that had received a single 8-mL dose of an NSAID within 2 months before being examined had no lesions visible on examination. Horses new to the facility were not more likely to have non-glandular ulcers. No significant differences were discovered among use or the four breed categories in either non-glandular ulcer severity scores or non-glandular ulcer number. There was a numerical trend for mean non-glandular ulcer number and mean non-glandular ulcer severity to be highest in horses used for training (17.4%), followed by horses used in polo (9.6%) and horses used in lessons (7.7%), respectively. Occurrence of non-glandular ulcers and severity of non-glandular ulcers differed across categories of age and gender (P < .05). Although we showed significant differences in these risk factors, the results should be interpreted with caution because of the small number of horses with gastric ulcers. No nonglandular ulcers were observed among the 8- to 17year-olds, whereas non-glandular ulcers occurred within 2 to 6-year-olds (21.4%), and 18- to 23-yearolds (16.7%). Mean non-glandular ulcer number and mean non-glandular ulcer severity score was higher (P < .05) among the 2- to 6-year-olds when compared with 18- to 23-year-olds. Mean non-glandular ulcer
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number and mean non-glandular ulcer severity score was higher (P < .05) among mares (19.3%) when compared with geldings (6.1%). DISCUSSION Others have reported that the most common location of gastric ulcers horses in training is within the squamous epithelial mucosa, with the most severe and greatest abundance of lesions occurring adjacent to the margo plicatus.5,9,10 All ulcerations in horses in this study were within the squamous epithelial mucosa adjacent to the margo plicatus. No glandular lesions were observed, however, the fluid or debris remaining in the stomachs of some of the animals, even after several hours of fasting, may have partially obscured our views of the glandular region. This study did not find a difference in the occurrence of non-glandular ulcers based on the breed of the horses studied. In a previous study, Thoroughbreds and Standardbreds were found to have a higher occurrence of gastric ulcers compared with Icelandic and Swedish Warmblooded horses.11 However, the number of affected horses in our study was much smaller, and making conclusions regarding the effect of breed is therefore difficult. The occurrence of ulcers among the three age groups was found to be significantly different, with no ulcers occurring in animals ranging in age from 8 to 17 years. A retrospective study of Swedish horses found that prevalence of gastric ulcerations decreased as animals aged.11 It has also been found that younger horses tend to be more susceptible to gastric ulcers.1,12,13 The results of this study appear to concur with the finding that gastric ulcers are common in young animals. Most non-glandular lesions occurred in the age group of 2- to 6-year-olds, primarily among the 3-year-olds. Three of the horses affected with non-glandular ulcers in our study population were 18 to 23 years old. The non-glandular ulcerations that occurred in the age group of 18to 23-year-olds occurred only in animals used in polo, which constituted 75% of this age group. Polo is an intense performance sport and exercise has been found to delay gastric emptying, subjecting the stomach to acid for a longer period, which may contribute to these horses’ susceptibility to gastric ulcers.2 A decrease in the amount of epidermal growth factor (EGF) produced by the salivary glands may lead to ulceration because it promotes cellular DNA synthesis and growth of the gastrointestinal mucosa.14 Again, with the small number of affected horses, whether this may also be true in the general population is difficult to say.
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A difference in occurrence of ulcers between mares and geldings was found within the population. Sandin et al found that, among the sexes, stallions and mares had a greater occurrence of ulcers (18% and 12%, respectively) when compared with geldings (10%).11 In a study in Thoroughbred racehorses, more females were affected with ulcers than males.13 In reproductively intact animals (mares and stallions), there may be a hormonal influence on the tissues, affecting their resistance to damage, making the gastric tissue more prone to developing lesions. In the study reported here, 19% of the mares had non-glandular ulcers, whereas only 6% of the geldings had non-glandular ulcers. We did not find a difference in non-glandular ulcer occurrence depending on the use of horses in our study. A previous study found that increased intra-abdominal pressure during exercise pushes gastric contents into the non-glandular portion of the stomach.15 These researchers postulate that the reason non-glandular ulcers tend to develop or worsen when horses are in intensive training programs is the duration of exposure to these acidic contents. The horses in training in our study do not undergo intensive training regimens. They are not worked for extended periods at the gallop but rather train for a short time at the walk, trot, and canter, with most of the time spent walking and trotting. The polo horses in our study are low-goal polo horses and therefore also may spend less time galloping than other groups that have been previously studied. The riding horses used in our study are involved in basic hunt seat lessons with some jumping and also are not ridden intensively (ie, at faster gaits such as the gallop) for extended periods. This could explain why the horses in our study had a considerably lower prevalence than other working categories of horses that have been examined. The prevalence of non-glandular gastric ulcers was 11% for horses in this study. Other studies have found a much higher occurrence of non-glandular gastric ulcers than the study discussed here. A previous study found that horses not in race training and used for riding lessons, pleasure, or show had a 37% prevalence of gastric ulceration.2,9 A study of Standardbred racehorses found an 87% prevalence of gastric ulceration.12 The greatest occurrence of gastric ulcers was found in Thoroughbred racehorses, ranging from 66% to 93%.1,13 Perhaps the closest in similarity to our study population would be show horses, horses retired from racing, and Western performance horses. However, the occurrence of non-glandular gastric ulceration in these populations was much higher—58%, 52%, and 40%, respectively.1,5,6 The horses in our study did not travel to
Journal of Equine Veterinary Science
May 2006
shows or competitions, and were used in their home environment. Previous studies of show horses and horses in a simulated show or training environment suggested that frequent traveling over long distances, frequent work, and the many environmental and dietary changes related to showing may have a negative influence on the ability of the gastric mucosa to withstand damage.5,7 In this study, the lack of extensive use for showing and other activities that would result in increased transportation and dietary and environmental changes possibly contributed to the low occurrence of non-glandular ulcerations found. All of the horses except the polo horses had access to pasture for 6 months before the study and were used mainly for light to moderate work. The three polo horses that had gastric ulcers had not had access to pasture for 6 months before the study. A previous study found that horses having outdoor access and access to pasture had normal stomachs.16 The statistical analysis in this study is based on a small number of horses with gastric ulcers, so the validity of the data could be questioned. However, there were statistical differences based on age and sex that correspond to pre-existing data in the literature. The study results suggest that horses used predominantly in their own environment, despite the frequency and intensity of activity, may have a lower occurrence of nonglandular gastric ulcers than previously studied mobile populations such as racing and show horses.
REFERENCES 1. 2.
Hammond CJ, Mason DK, Watkins KL. Gastric ulceration in mature Thoroughbred horses. Equine Vet J 1986;18:284-287. Murray MJ, Grodinsky C, Anderson CW, Radue PF, Schmidt GR. Gastric ulcers in horses: a comparison of endoscopic findings in
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3.
4. 5. 6. 7. 8. 9. 10. 11.
12.
13. 14.
15. 16.
horses with and without clinical signs. Equine Vet J Suppl 1989;7:68-72. Vatistas NJ, Snyder JR, Carlson G, Johnson B, Arthur RM, Thurmond M, Lloyd KCK. Epidemiological study of gastric ulceration on the Thoroughbred racehorse: 202 horses 1992-1993. Proc 40th Annual Convention American Association Equine Practitioners 1994;125-126. 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. McClure SR, Glickman LT, Glickman NW. Prevalence of gastric ulcers in show horses. J Am Vet Med Assoc 1999;215:1130-1133. Bertone JJ. Prevalence of gastric ulcers in elite, heavy use western performance horses. Proc 46th Annual Convention American Association Equine Practitioners 2000;256-259. McClure SR, Carithers DS, Gross SJ, Murray MJ. Gastric ulcer development in horses in a simulated show or training environment. J Am Vet Med Assoc 2005; 227:775-777. MacAllister CG, Andrews FM, Deegan E, Ruoff W, Olovson SG. A scoring system for gastric ulcers in the horse. Equine Vet J 1997;29,430-433. Furr MO, Murray MJ. Treatment of gastric ulcers in horses with histamine type 2 receptor antagonists. Equine Vet J Suppl 1989;7:77-79. Murray MJ. Gastric ulcers in adult horses. The Compendium 1994;792-794,797. Sandin A, Skidell J, Häggström J, Girma K, Nilsson G. Postmortem findings of gastric ulcers in Swedish horses older than age one year: a retrospective study of 3715 horses (1924-1996). Equine Vet J 2000;32:36-42. 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. Murray MJ, Schusser GF, Pipers FS, Gross SJ. Factors associated with gastric lesions in Thoroughbred racehorses. Equine Vet J 1996;28:368-374. Gysin B, Muller RKM, Otten U, Fishlie AE. Epidermal growth factor content of submandibular glands is increased in rats with experimentally induced gastric lesions. Scand J Gastroenterol 1988;23:665-671. Lorenzo-Figueras M, Merritt AM. Effects of exercise on gastric volume and pH in the proximal portion of the stomach of horses. Am J Vet Res 2002;63:1481-1487. Murray MJ. Equine model of inducing ulceration in alimentary squamous epithelial mucosa. Dig Dis Sci 1994;39:2530-2535.
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