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Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment
Journal of Equine Veterinary Science xxx (2019) 102742
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Original Research
Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment Nanna Luthersson a, *, Coby Bolger b, Paloma Fores c, Clare Barfoot d, Sarah Nelson d, Timothy Parkin e, Pat Harris f a
Hestedoktoren I/S, Kr. Eskilstrup, Denmark Horse1 e Equine Nutrition Centre, Leganes, Madrid, Spain Universidad Complutense de Madrid, Spain d MARS Horsecare UK, Milton Keynes, Slough, Berkshire, UK e Boyd Orr Centre for Population and Ecosystem Health, School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK f Equine Studies Group, WALTHAM Centre for Pet Nutrition, Leics, UK b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 11 February 2019 Received in revised form 2 May 2019 Accepted 6 May 2019 Available online xxx
Diet is an accepted risk factor for equine squamous gastric disease (ESGD), but there is little published evidence for the benefit of dietary change (DC). This study evaluated the effect of DC with or without initial omeprazole medication. Twelve pairs of exercising horses with ESGD Grade 2/4 (EM) and 17 pairs with ESGD Grade 3/4 (ES), were monitored. Paired horses had similar management, feeding times, workloads, and initially feed or forage. One of each pair was randomly assigned, postgastroscopy (Scope1), to a specified restricted starch ration; the other remained on their original diet. Omeprazole (4 mg/kg per os SID) was given to all ES pairs for 4 weeks. Gastroscopies were scored, without dietary knowledge, after 4 and 10 weeks (Scopes 2 and 3). Workloads remained similar throughout. McNemar’s tests identified any changes in ESGD grade. Within the EM group, DC had no additional effect. For the ES group remaining on their original diet, there was significant improvement in ESGD grade from Scopes 1 to 2 (P < .001) but a worsening between Scopes 2 and 3 (P ¼ .005), with Scope 3 being no different from Scope 1 (P ¼ .08) reflecting no apparent long-term medication benefit. For the DC group, there was significant improvement in ESGD grade from Scopes 1 to 2 (P < .001) and between Scopes 1 and 3 (P ¼ .003); In addition, there was no significant difference between Scopes 2 and 3 (P ¼ .32). Although limited by the small number of pairs evaluated, this study provides evidence that appropriate DCs can be a beneficial management strategy for ESGD. © 2019 Elsevier Inc. All rights reserved.
Keywords: EGUS ESGD Nutrition Starch Omeprazole Prevention
1. Introduction The horse, as a nonruminant herbivore, evolved to ingest a highfiber, low-starch diet through daily (up to 18 hours) foraging. Modern management practices, including meal feeding and low-
Animal welfare/ethical statement: Ethical permission was obtained from the Communidad de Madrid for the study. Conflict of interest statement: P.H., C.B., and S.N., work for Mars Horsecare who commercially produce the feeds used in this trial, and C.B. distributes them in Spain. P.H., C.B., S.N., and C.B. were not involved in the EGUS scoring or the data analysis. * Corresponding author at: Hestedoktoren I/S, Hvalsovej 298, Kr. Eskilstrup 4360, Denmark. E-mail address: [email protected] (N. Luthersson).
fiber or high-starch and sugar-rich diets, increase the risk of developing a poorly buffered, acidic gastric environment and a high prevalence of the Equine Gastric Ulcer Syndrome (EGUS) [1e3]. The incidence of EGUS, especially in actively training and exercising animals, is up to 90% depending on the inclusion criteria [2,3]. Several risk factors have been identified [1,4], in particular, nutrition (e.g., low-fiber intake, long gaps between forage provision, the feeding of starch-rich complementary feeds [2e4]), although there is currently more evidence in support of the role of nutrition and management for the risk of equine squamous gastric ulcers (ESGD) than equine glandular gastric ulcers (EGGD) [3,4]. However, few studies have actually evaluated the effect of a change in nutritional management on the recovery from EGUS, especially postmedical treatment. Recent studies have highlighted that there is often gastric ulceration recurrence post or even during long-term
https://doi.org/10.1016/j.jevs.2019.05.007 0737-0806/© 2019 Elsevier Inc. All rights reserved.
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
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N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
pharmacologic treatment, and this might be where changes in nutrition and managemental practices can perhaps play a very important role. The long-term study of Kerbyson et al [5], for example, found that a proportion of the horses had the same or higher ulcer score after 90 days, compared with their starting point, despite long-term administration of omeprazole or a supplement (with no other designed change in management or nutrition). Other changes may be required, therefore, in addition to the use of pharmaceutical agents or nutritional supplements, to manage EGUS. We hypothesized that appropriate nutritional changes would help maintain gastric health during and postmedical treatment. This field study was therefore undertaken with the following goals: (1) to evaluate the effect of dietary change (DC) in conjunction with medical treatment, where clinically appropriate, on ESGD lesions and (2) to evaluate the effect of maintaining the DC on squamous gastric ulceration following cessation of the medical treatment. 2. Materials and Methods 2.1. Study Design All horses underwent an initial gastroscopy following 15e18 hours of feed and forage (but not water) withdrawal. A complete evaluation of the nonglandular region of the stomach was undertaken, and a record of any lesions made using the EGUS Council severity scoring system (0e4/4) [2]. Animals included in the study (Grade 2e4/4 Ulcers) were paired initially according to their grade of ESGD lesion and were as similar as possible in their workloads and management. Workloads were grouped as follows: rest to light: horse only walking and trotting; light to moderate: up to 1 hour of work per day with competitions not more than 2 weekends per month, for example, racehorses not racing but in fitness work, those competing in show jumping and horseball; hard work: racehorses in active racing with fast work done at least twice a week. Where pairs could not be found within the exact workload grouping, the closest match to their individual exercise load was found (n ¼ 2). The horse identification numbers were individually listed on sheets of paper, which were then shuffled and then alternatively chosen to be put into the change or no change group. The horses allocated to the “change feed category” were all introduced onto the trial complementary feed. Horses that did not change diet continued with their usual feed, forage, and management. The trial complementary feed provided a similar estimated energy intake to their normal ration and was introduced over a 5e7 days acclimatization period. At one establishment, five horses in the change diet group also had their forage changed from straw only to meadow hay. All other horses in the change diet group remained on their prestudy forage. The protocol requested that all horses, regardless of whether or not the feed was changed, continued at their pretrial exercise level and maintained their competition schedule throughout the study. All owners reported similar work levels throughout the trial, except for 3 animals whose work levels varied due to issues unrelated to the study. All animals with ESGD Grades 3 and 4/4 were given the recommended dose of omeprazole (4 mg/kg per os once a day) for 4 weeks after which a repeat gastroscopic evaluation (Scope 2) was undertaken (within 24 hours of stopping the treatment). The horses then continued on their respective dietary regimens for a further 6 weeks at which point the final gastroscopic evaluation was made (Scope 3). Horses with ESGD Grade 2 lesions were not given any omeprazole but were still gastroscoped after 4 and 10 weeks. Any omeprazole dose was administered first thing in the morning before any forage or complementary feed had been given.
Body weight (BW) was estimated using a commercial heightspecific weight tape [6] before each gastroscopy. 2.2. Horses and Venues Ninety-nine horses (32 Thoroughbreds, 63 Warmblood sport horses, and four ponies; BW average 461 kg (range 277e600 kg), body condition score (BCS) median 5.5/9 (range 3e7/9) were initially scoped at four establishments, which for practical reasons were in close geographical proximity (within a 70 km area around Madrid), followed similar management practices, and fed (3 out of the 4 establishments) hay/haylage from the same source and supplier. The fourth establishment fed straw as the only forage. They were used for racing (n ¼ 26) and dressage (n ¼ 24) and show jumping (n ¼ 23) and horseball (n ¼ 26). Five horses had no evidence of any gastric lesions, one just had glandular ulcers, 17 had Grade 1 ulceration (17%), and 76 (77%) had ESGD ulcers Grades 2. For 10 of these 76 animals, an appropriate pair could not be found; therefore, 66 horses started the feeding study. A total of 58 (18 Thoroughbreds, 36 Warmblood sport horses, and four ponies; 12 aged between 2 and <4 years; 12 aged between 4 and <8 years; 32 aged between 8 and <14 years; and 2 animals aged >14 years) completed the whole protocol and participated fairly evenly across the four activities. The eight animals that did not complete the study were sold by their owners and left the area and were therefore lost to follow-up. Four came from the no change group and four from the change group, and two were already paired. The remaining horses were again primarily paired according to their gastric ulcer grade but also their workload and original diets. None of the horses had been studied or diagnosed as having any sort of ulcer before the study. 2.3. Management and Nutritional Information Key details of the training, management, and nutrition of the above horses before the start of the study were obtained. Their current digestible energy intake was estimated (based on manufacturer information or reference texts) and, for the horses that would be changing onto the trial complementary feed, an appropriate isocaloric intake from the study diet was determined. The trial complementary feed was a 50:50 mix of two proprietary complementary feeds (WINERGY Equilibrium Growth and SPILLERS HDF Power Cubes; MARS Horsecare UK Ltd) and was directed to be fed in three meals per day. Representative composite samples of the original diets (forage and complementary feeds) were sent for analysis by wet chemistry for starch, water-soluble carbohydrate (WSC), dry matter, and neutral detergent fiber (NDF) by Equi-Analytical of Dairy One. Nonstructural carbohydrate intake (NSC) was calculated as the starch plus WSC. 3. Statistical Analyses McNemar’s tests for all horses and each group (feed change or not) were performed using EGSD score of 2 or 3 as being clinically significant. McNemar’s tests were also used to identify changes in EGSD grade for both groups between Scopes 1 and 2; 1 and 3; 2 and 3 for horses initially graded as EGSD 2 (EM) and for horses initially graded as EGSD >2 (ES). Two different cut-offs at Grades 2 and 3 were used to dichotomize the ordinal ESGD scale. Normality tests were conducted on continuous data relating to original and trial diet composition and for weight data. Body condition score data were treated as if nonparametric. Wilcoxon sign rank or paired t-tests were conducted to identify differences in the dietary composition following a change in diet for those horses that
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
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Table 1 Starch, nonstructural carbohydrate (NSC), and neutral detergent fiber (NDF) intakes from the complementary feed only: mean (and range). Starch Content in Diet
Mean (Range), Starch g/kg, BW/d
Mean (Range), NSC g/kg, BW/d
Mean (Range), NDF g/kg, BW/d
Original diets for all horses Original diets for those horses that changed diet Following change in diet for those horses that changed diet
3.49 (0.48e6.37) 3.50 (0.77e5.98) 0.94 (0.33e1.55)
4.29 (0.97e7.72) 4.31 (1.29e7.31) 1.68 (0.60e2.78)
3.65 (1.01e8.05) 3.50 (1.19e7.53) 3.37 (1.21e5.58)
Abbreviation: BW, body weight.
changed diet. These analyses were performed for the trial diet alone and the trial diet and forage together. Wilcoxon sign rank or paired t-tests were also conducted to identify change in estimated BW and BCS in the two diet change or no diet change groups between Scopes 1 and 2, 1 and 3, and 2 and 3. Fisher exact tests were used to identify differences in any changes in behavior reported by owners in horses in each group (feed change or not). This analysis was performed separately for those horses that started the trial with an EGSD score of 2 and also for those horses that started the trial with an EGSD score of 3.
4.3. Nutrition
Fifty-five of the 58 animals maintained the same intensity and level of work throughout the study. However, one increased and two reduced their level of work for reasons unrelated to the study. Of the 29 horses that changed diet, 28 maintained the same workload, 0 increased and 1 reduced workload, and for those horses that did not change diet, 27 maintained the same workload and 1 increased and 1 reduced workload. The disciplines of the participant horses were also as evenly distributed as possible between the group that changed diets and the group that continued on the same diet. Nine racehorses, eight horseball horses, eight dressage horses, and four show jumpers had their diets changed to the study diet. The group that did not change diet consisted of seven racehorses, nine horseball horses, seven dressage horses, and six show jumpers.
At the start of the study, the nutritional intake from the complementary feeds being fed varied considerably as shown in Table 1. All horses received at least one commercial product, and for 33/58, the complementary feeds were provided twice a day, and the rest were fed three meals. For 17 (out of 29) animals that changed diet, the change in diet also meant an increase in the number of meals per day from two to three (all the others were already being fed their complementary feed ration in three meals). Meal timings otherwise remained consistent between the pairs throughout the study. None of the horses included in the study had access to pasture or paddock of any kind. Six different hays and one haylage were fed (mean intake 10.3gDM/kg BW/day; range 3.05e21.18) together with a variety of chaffs at the start of the study. The estimated dietary intake when combined with the complementary feed was as shown in Table 2 (ad libitum provision of forage was taken as providing 2% BW in dry matter. No allowance was made for any intake of any bedding. Any fiber-based balancer or chaff that was originally fed to the change in diet group was removed when they received the study diet. For one establishment, straw was fed as the only forage; therefore, for the five pairs based at this establishment, the change in diet also included changing to the hay provided by another study establishment. The core type of forage fed by each establishment remained the same over the study period, and any changes in forage batch fed were the same for each animal within a pair (i.e., same for those that had had their diet changed and those that did not). Whether examining the complementary feed alone or the complementary feed with forage, there were significant reductions in starch and NSC intake (P values < .001), but not NDF following the change of diet.
4.2. BW and BCS
4.4. Behavior
There was no significant change in estimated BW for those 58 animals that completed the study (455 ± 70; 447 ± 71; 443 ± 66 kg at the three gastroscopies, respectively) or between any of the scopes for either group of horses. In the group that did not change diet, there was a slight increase in BCS (median: 5e5.5; P value ¼ .04) between Scopes 2 and 3. In the group that did change diet, the median BCS at Scopes 1, 2, and 3 were 5.5, 5.5, and 5, respectively. There were statistically significant differences in all comparisons in BCS in this group for between Scopes 1 and 2 (P value ¼ .04), between Scope 1 and 3 (P value < .001), and between Scopes 2 and 3 (P value ¼ .006).
Initially, owners, riders, or trainers were asked if they felt their horse was healthy and how they felt about their horses’ physical appearance or behavior. Thirty-seven (64%) felt that their horses were healthy and made no comment; three owners said that they felt that their horses looked “poorly” with a lack of coat shine; six owners reported that their horses suffered occasional unexplainable colics; five reported that the horse was underweight; three commented that their horses suffered from fecal water syndrome; two reported the horses as “stressed”; one reported the horse as having a lack of appetite; one horse had been diagnosed with recurrent equine rhabdomyolysis, and another had been diagnosed
4. Results There were no clinical issues or other problems associated with the gastroscopies, and the DCs were well accepted in all 29 horses assigned to the “change diet” group. 4.1. Workload and Disciplines
Table 2 Starch, nonstructural carbohydrate (NSC), and neutral detergent fiber (NDF) intakes from the complementary feed and forage: mean (and range). Starch Content in Diet
Mean (Range), Starch g/kg, BW/d
Mean (Range), NSC g/kg, BW/d
Mean (Range), NDF g/kg, BW/d
Original diets for all horses Original diets for those horses that changed diet Following change in diet for those horses that changed diet
3.62 (0.93e6.41) 3.61 (0.93e6.02) 1.05 (0.49e1.94)
5.51 (2.90e8.23) 5.60 (3.20e8.23) 3.03 (1.42e5.36)
9.77 (3.69e16.72) 9.49 (3.69e16.21) 9.57 (4.89e22.9)
Abbreviation: BW, body weight.
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
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N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
with chronic piroplasmosis (although both of these horses were in full work and competing). At the second and third scoping, the owners were asked simply whether each individual horse had shown any change in their overall behavior or physical appearance and whether any such change was perceived as positive or negative. For the horses that started the trial with ESGD score of 2, there was a statistically significant difference in owner reported behavior change at the third scope when comparing a positive behavior change with negative or no change (P value ¼ .009). In this group, 8 of 12 horses on the trial diet had a positive behavior change, whereas only 1 of 12 horses that did not change diet was reported as having a positive behavior change. Other similar comparisons were not statistically significant. 4.5. Equine Squamous Gastric Disease Of the 58 animals that completed the study, at Scope 1, 24 had Grade 2 ulcers, 23 Grade 3 and 11 Grade 4 ulcers. One animal in the change diet group and one animal without a change in diet within the Grade3/4 ulcer group were not able to be scoped on the second occasion for competition reasons. Their data were removed for evaluating the efficacy of omeprazole and post omeprazole DC. As horses were paired based on the severity of ESGD score at the start of the study, there was no statistical difference in initial ESGD grade between the groups that undertook the DC or did not. 4.5.1. Looking at All Animals In both feed groups, there was a significant difference in ESGD score of 2 prevalence between Scopes 1 and 2 and between Scopes 1 and 3 (all P values < .001; Fig. 1). Regardless of feed change status, there was a significant reduction in the prevalence of ESGD score of 2 at Scopes 2 and 3 compared with at Scope 1. A difference between the two feed change groups was identified when comparing the change in ESGD score of 2 prevalence at Scopes 2 and 3: For those that changed diet: There was no significant difference in the prevalence of ESGD score of 2 prevalence at Scopes 2 and 3 (P value ¼ 1.0): 18 horses were ESGD 2 at Scope 2 AND <2 at Scope 3; three went from 2 to <2; three stayed at 2; four horses went from <2 to 2. For those that did not change diet: There was a significant difference in the prevalence of EGSD score of 2 prevalence at Scopes 2 and 3 (P value ¼ .027): 14 horses were EGSD <2 at
No diet change 4.5
Diet change
4 3.5
ESGD score
3 2.5 2 1.5 1 0.5 0 1
2
3
Scope number Fig. 1. Number of horses (represented by the size of the bubble) with each ESGD score at the start at each scoping for the two feed groups. An increase in the size of the bubble therefore reflects and increase number of animals at that score and vice versa.
Scope 2 AND <2 at Scope 3; one went from 2 to <2; three stayed as 2; 10 horses went from <2 to 2.
4.5.2. Grade 2 Ulcers Only For the 12 horses with Grade 2 ulcers that changed diet, there was a significant difference in ESGD score between Scopes 1 and 2 (P value ¼ .03) and Scopes 1 and 3 (P value ¼ .02). For the initial Grade 2 horses that did not change diet, there were also significant differences in ESGD score between Scopes 1 and 2 (P value ¼ .004) and Scopes 1 and 3 (P value ¼ .01). For neither group were there significant differences in EGSD score between Scopes 2 and 3 (P values ¼ .45 and .55, respectively). 4.5.3. Grade 3 and 4 Ulcers Only For the 17 pairs of horses with Grade 3 or 4 ulcers there was a significant effect of the omeprazole with all but one animal showing an improvement over the course of the treatment: three animals improved by 1 grade; 12 by 1.5e2 grades; 13 by 2.5e3 grades; and three by four grades with only one staying the same. Over the two groups, there was 81% good healing to a score of 0/1, with 13% moderate healing (to a score 2) and 6% showed no healing. For the no diet change group, there was a significant improvement from Scope 1 to Scope 2 (P < .001), but a significant worsening between Scopes 2 and 3 (P ¼ .005) and ultimately no significant difference from Scope 1 to 3 (P ¼ .08) that is no apparent long-term effect of the medical treatment. For the diet change group, there was a significant improvement from Scope 1 to Scope 2 (P < .001), and there was no significant difference between Scopes 2 and 3 (P ¼ .32), and there remained a significant difference from Scope 1 to 3 (P ¼ .003). This is illustrated in Fig. 2. At Scope 3, only three horses in the no diet change group were ESGD grade <2, whereas nine horses in the diet change group were ESGD grade <2. Of the five horses that had their complementary feed and forage changed, only two of them started with a Grade 3 ulcer, and both improved slightly following omeprazole. One of these animals continued to improve post cessation of treatment and one slightly worsened. 5. Discussion This, to the authors’ knowledge, is the first article to look at the effect of DC on the healing and recurrence of ESGD. The study confirmed that >80% of horses with Grade 3 or 4 ulcers responded well to omeprazole with respect to their ESGD with no additional positive or negative effect of DC. Six weeks after omeprazole treatment without DC, there was overall a worsening of gastric health so that, by the end of the trial, these animals overall were no different from the start (i.e., there was no long-term benefit of the omeprazole treatment). However, overall, those that changed diet remained significantly improved at the end of the trial suggesting an advantage of making these DCs. This would suggest that, especially when changes in management and training level are not feasible, making appropriate changes in the ration may be of value. There was no apparent effect of the change in diet on gastric ulceration in animals with ESGD Grade 2, although interestingly the owners or feeders subjectively reported some improvements in behavior [7], perhaps related to the reduction in starch or NSC intake. This was not reported with the higher grade ulcers, however, and suggests additional work is needed to explore this more fully. The response to omeprazole treatment was similar to that expected in the field [8]. The level of recurrence post omeprazole treatment was also as expected and confirms that dietary, training, or other environmental factors drive ulcer formation and that a
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
No diet change 4.5
Diet change
4 3.5
ESGD score
3 2.5 2 1.5 1 0.5 0 1
2
Scope number
3
Fig. 2. Number of horse (represented by the size of the bubble) at each scoping in the two diet groups that started with an ESGD score of 3 or 4/4. An increase in the size of the bubble therefore reflects and increase number of animals at that score and vice versa.
course of omeprazole acts, as expected, purely as a treatment, not as a long-term preventative agent. A range of different complementary feeds were provided to the animals at the start of the diet although many of the rations were based on manufactured feeds rather than home-mixed rations. A high proportion of the animals (17/29) that changed diet also had an increase in the number of meals per day (from two to three: all the others were already being fed their complementary feed ration in three meals), which may been additionally advantageous due to reduced starch intake per meal [4]. Further studies in larger numbers of animals would be needed to further tease out which specific changes in the ration are the main drivers of the benefit seen here. Forage provision remained the same within each pair as did the management and training as far as possible. For animals at three of the four establishments, the change in diet meant purely a change in the complementary component of the ration not the type or timing or amount of forage being provided. However, all these establishments were already feeding some form of hay or haylage. For one of the establishments, which was originally feeding straw, the change diet horses were also moved onto the same meadow hay that was being fed at two of the other establishments. This only affected five pairs of animals and for the five that changed their forage (as well as their complementary feed) only two had Grade 3 ulcers at the start, one of which continued to improve and the other regressed slightly; therefore, this did not apparently influence the overall results. Feeding predominantly straw as the forage has been shown to be a major nutritional risk factor to gastric ulcer formation [4], therefore, it seemed appropriate to make this change although it did not have any apparent effect on the results. The amount and timing of the forage were not changed at any establishment (as far as we know), and overall, the NDF intake did not change with the change in diet. Given the overall low-forage intake, it is therefore possible that even greater differences between the diet change and no diet change groups may have been seen if the forage component of the ration had also been further addressed (amount/timing) in the diet change group. The chosen study complementary feed diet is a ration that has been practically recommended for use in high-performance horses, and certainly, there was no effect on estimated BW. There was a slight decrease in body condition in the change diet group (compared with a slight increase in the no change group), suggesting perhaps some difference in the body composition in the two groups or reflecting the subjective nature of BCS especially around the 5e5.5/9 score. There were no reported adverse effects
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on performance despite the significant overall reduction in starch and NSC intake. Recent studies have suggested that forage-only diets can be used to meet the high energy requirements of horses in very heavy training [9], providing their energy provision is high enough, although questions over glycogen restoration persist. Key nutritional recommendations for reducing the risk of gastric ulceration are fundamentally based on studies comparing the diets of animals that do have and do not have ulcers and assessing the risk [4]. This is the first study to suggest that rations based on these principles (i.e., principally reduced starch or NSC intake per day and per meal) may be beneficial following medical treatment. Although the study diet provided overall significantly lowered starch intake per day and per meal (as can be seen from the original range of intakes); some animals with ulcers were already on a low daily starch intake of <1 g/kg BW per day, suggesting that although this aspect of the diet may play a role in ulcer formation, it is not the only potential causative agent. Also while a statistical difference with respect to Grade 3 or 4 lesions was shown between the responses of those with and without change in diet, the numbers were insufficient to explore whether the individual differences in response were associated with their initial diet or not. The study diet provided some other suggested nutritional components to reduce the risk of ulcer including a small amount of alfalfa chaff and additional oil [10], which may have also played a role. It has been suggested that calcium and protein, both high in alfalfa hay, buffer stomach contents, resulting in a protective effect on the squamous mucosa [3,11]. In contrast, recent work has suggested that certain forms of alfalfa chaff fed in very large amounts may increase the risk of EGGD perhaps due to mechanical damage [12,13]. As some alfalfa chaff was included in the study diet it was recorded as either yes or no at the start and end (with yes: taken as there being a significant lesion, with erosion or ulceration, of the glandular mucosa, and no: where there was no or only a minor change in the glandular mucosa with no visible pathology or erosion/ulceration), stating whether EGGD lesions were present that could potentially be considered to be of significance. Of those animals that completed the study and whose glandular region could be fully evaluated: 27 had some evidence of glandular lesions at the start, and 18 at the end of the study (10 with change in diet and 8 with no change). Six animals originally free from glandular ulcers had evidence of some glandular lesions by the end of trial (four on the changed diet and two on the no changed diet), whereas 22 animals negative for EGGD at the start were also negative at the end (11 with change in diet and 11 with no change). No firm conclusions can be drawn, other than there was no apparent noticeable adverse effect of the diet change on EGGD, especially as currently it is very difficult to assess EGGD over time with respect to severity, due to little correlation between endoscopic findings and histopathology [14]. In addition, the omeprazole was not given according to new recommendations for EGGD lesions [15,16]. This was a field trial, and while it may be more applicable to real life situations, it did mean that for logistical reasons the numbers of animals initially scoped was restricted to nearly 100. Although all but six did have evidence of ESGD, 17 only had lesions reported as Grade 1. Horses with such level of ulceration were not included as it was considered that it would be difficult to clearly define and show improvement or deterioration with such individuals. The relatively small numbers of animals (58) completing the whole study is an obvious limitation of this study. It is known for example that the workload is an important risk factor (2, 3) for ESGD, but there were not enough horses available in the area with the required ulcer score, the same discipline, and workload to form statistically significant discipline or workload groups. Obviously, the type of training and exercise will vary between racing and sporting horses; therefore, the groups were spread as evenly as possible primarily by
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
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N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
ESGD score, then by workload and then as far as possible by discipline. In addition, by ensuring that the two animals within each pair were kept under similar management regimens as each other, it was hoped that other extrinsic potential EGUS risk factors would remain the same for those that changed diet and those that did not. However, this remains a limitation, and it is recommended that future work should evaluate further the relative efficacy of DC postmedical treatment cessation according to both discipline and workload.
6. Conclusions Despite the limitations and challenges related to field trials, this study is the first to provide evidence that appropriate DCs can be a beneficial management strategy for those with more severe ESGD. Further work is needed to evaluate the added benefits of improving forage provision.
Acknowledgments The authors thank the owners and their vets who trusted us with their wonderful horses and Christina Dominguez for helping us organize all the work at the Madrid racetrack. They also thank s, Dorka Fulop, vet students and apprentices, Manuel San Andre n, Atocha Calvo, and Maria Clara Colmenero, Alejandro Mercha Alonso, for tirelessly helping with so many aspects that needed to be handled to get this study done.
Financial disclosures n para Financial support for this study was provided by Fundacio la Promocion del Deporte Ecuestre, ScanVet Animal Health A/S, Norbrook Laboratories Limited, WALTHAM, and Mars Horsecare UK.
References [1] Murray MJ, Schusser GF, Pipers FS, Gross SJ. Factors associated with gastric lesions in Thoroughbred racehorses. Equine Vet J 1996;28:368e74. [2] Sykes BW, Hewetson M, Hepburn RJ, Luthersson N, Tamzali Y. European College of Equine internal Medicine consensus statement: equine gastric ulcer syndrome in adult horses. J Vet Intern Med 2015;29:1288e99. [3] Andrews FM, Larson C, Harris P. Nutritional management of gastric ulceration. Equine Vet Educ 2017;29:45e55. [4] Luthersson N, Hou Nielsen K, Harris P, Parkin TDH. Risk factors associated with equine gastric ulceration syndrome in 201 horses in Denmark. Equine Vet J 2009;41:625e30. [5] Kerbyson NC, Knottenbelt DK, Carslake HB, Conwell RC, Sutton DGM, Parkin TDH. A comparison between omeprazole and a dietary supplement for the management of squamous gastric ulceration in horses. J Equine Vet Sci 2016;40:94e101. [6] Ellis JM, Hollands T. Use of height-specific weigh tapes to estimate the bodyweight of horses. Vet Rec 2002;150:632e4. [7] Malmkvist J, Poulsen JM, Luthersson N, Palme R, Christensen JW, Søndergaard E. Behaviour and stress responses in horses with gastric ulceration. Appl Anim Behav Sci 2012;142:160e7. [8] Sykes BW, Sykes KM, Hallowell GD. A comparison of two doses of omeprazole in the treatment of equine gastric ulcer syndrome: a blinded, randomised, clinical trial. Equine Vet J 2014;46:416e21. [9] Ringmark S, Roepstorff L, Hedenstrom U, Lindholm A, Jansson A. Reduced training distance and a forage-only diet did not limit race participation in young Standardbred horses. Comp Exerc Physiol 2017;13:265e72. [10] Cargile JL, Burrow JA, Kim I, Cohen ND, Merritt AM. Effect of dietary corn oil supplementation on equine gastric fluid acid, sodium, and prostaglandin E2 content before and during pentagastrin infusion. J Vet Intern Med 2004;18: 545e9. [11] Nadeau JA, Andrews FM, Mathew AG, Argenzio RA, Blackford JT, Sohtell M, Saxton AM. Evaluation of diet as a cause of gastric ulcers in horses. Am J Vet Res 2000;61:784e90. [12] Vondran S, Venner M, Vervuert I. Effects of two alfalfa preparations with different particle sizes on the gastric mucosa in weanlings: alfalfa chaff vs. alfalfa pellets. BMC Vet Res 2016;12:110. [13] Vondran S, Venner M, Coenen M, Vervuert I. Effects of alfalfa chaff on the gastric mucosa in adult horses. Pferdeheilkunde 2017;33:66e71. [14] Martineau H, Thomson H, Taylor D. Pathology of gastritis and gastric ulceration in the horse. Part 1: range of lesions present in 21 mature individuals. Equine Vet J 2009;41:638e44. [15] Sykes BW, Sykes KM, Hallowell GD. A comparison of three doses of omeprazole in the treatment of equine gastric ulcer syndrome: a blinded, randomized, doseeresponse clinical trial. Equine Vet J 2015;47:285e90. [16] Sykes BW, Underwood C, Greer R, McGowan CM, Mills P. The effects of dose and diet on the pharmacodynamics of omeprazole in the horse. Equine Vet J 2016;49:525e31.
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
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Original Research
Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment Nanna Luthersson a, *, Coby Bolger b, Paloma Fores c, Clare Barfoot d, Sarah Nelson d, Timothy Parkin e, Pat Harris f a
Hestedoktoren I/S, Kr. Eskilstrup, Denmark Horse1 e Equine Nutrition Centre, Leganes, Madrid, Spain Universidad Complutense de Madrid, Spain d MARS Horsecare UK, Milton Keynes, Slough, Berkshire, UK e Boyd Orr Centre for Population and Ecosystem Health, School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK f Equine Studies Group, WALTHAM Centre for Pet Nutrition, Leics, UK b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 11 February 2019 Received in revised form 2 May 2019 Accepted 6 May 2019 Available online xxx
Diet is an accepted risk factor for equine squamous gastric disease (ESGD), but there is little published evidence for the benefit of dietary change (DC). This study evaluated the effect of DC with or without initial omeprazole medication. Twelve pairs of exercising horses with ESGD Grade 2/4 (EM) and 17 pairs with ESGD Grade 3/4 (ES), were monitored. Paired horses had similar management, feeding times, workloads, and initially feed or forage. One of each pair was randomly assigned, postgastroscopy (Scope1), to a specified restricted starch ration; the other remained on their original diet. Omeprazole (4 mg/kg per os SID) was given to all ES pairs for 4 weeks. Gastroscopies were scored, without dietary knowledge, after 4 and 10 weeks (Scopes 2 and 3). Workloads remained similar throughout. McNemar’s tests identified any changes in ESGD grade. Within the EM group, DC had no additional effect. For the ES group remaining on their original diet, there was significant improvement in ESGD grade from Scopes 1 to 2 (P < .001) but a worsening between Scopes 2 and 3 (P ¼ .005), with Scope 3 being no different from Scope 1 (P ¼ .08) reflecting no apparent long-term medication benefit. For the DC group, there was significant improvement in ESGD grade from Scopes 1 to 2 (P < .001) and between Scopes 1 and 3 (P ¼ .003); In addition, there was no significant difference between Scopes 2 and 3 (P ¼ .32). Although limited by the small number of pairs evaluated, this study provides evidence that appropriate DCs can be a beneficial management strategy for ESGD. © 2019 Elsevier Inc. All rights reserved.
Keywords: EGUS ESGD Nutrition Starch Omeprazole Prevention
1. Introduction The horse, as a nonruminant herbivore, evolved to ingest a highfiber, low-starch diet through daily (up to 18 hours) foraging. Modern management practices, including meal feeding and low-
Animal welfare/ethical statement: Ethical permission was obtained from the Communidad de Madrid for the study. Conflict of interest statement: P.H., C.B., and S.N., work for Mars Horsecare who commercially produce the feeds used in this trial, and C.B. distributes them in Spain. P.H., C.B., S.N., and C.B. were not involved in the EGUS scoring or the data analysis. * Corresponding author at: Hestedoktoren I/S, Hvalsovej 298, Kr. Eskilstrup 4360, Denmark. E-mail address: [email protected] (N. Luthersson).
fiber or high-starch and sugar-rich diets, increase the risk of developing a poorly buffered, acidic gastric environment and a high prevalence of the Equine Gastric Ulcer Syndrome (EGUS) [1e3]. The incidence of EGUS, especially in actively training and exercising animals, is up to 90% depending on the inclusion criteria [2,3]. Several risk factors have been identified [1,4], in particular, nutrition (e.g., low-fiber intake, long gaps between forage provision, the feeding of starch-rich complementary feeds [2e4]), although there is currently more evidence in support of the role of nutrition and management for the risk of equine squamous gastric ulcers (ESGD) than equine glandular gastric ulcers (EGGD) [3,4]. However, few studies have actually evaluated the effect of a change in nutritional management on the recovery from EGUS, especially postmedical treatment. Recent studies have highlighted that there is often gastric ulceration recurrence post or even during long-term
https://doi.org/10.1016/j.jevs.2019.05.007 0737-0806/© 2019 Elsevier Inc. All rights reserved.
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
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N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
pharmacologic treatment, and this might be where changes in nutrition and managemental practices can perhaps play a very important role. The long-term study of Kerbyson et al [5], for example, found that a proportion of the horses had the same or higher ulcer score after 90 days, compared with their starting point, despite long-term administration of omeprazole or a supplement (with no other designed change in management or nutrition). Other changes may be required, therefore, in addition to the use of pharmaceutical agents or nutritional supplements, to manage EGUS. We hypothesized that appropriate nutritional changes would help maintain gastric health during and postmedical treatment. This field study was therefore undertaken with the following goals: (1) to evaluate the effect of dietary change (DC) in conjunction with medical treatment, where clinically appropriate, on ESGD lesions and (2) to evaluate the effect of maintaining the DC on squamous gastric ulceration following cessation of the medical treatment. 2. Materials and Methods 2.1. Study Design All horses underwent an initial gastroscopy following 15e18 hours of feed and forage (but not water) withdrawal. A complete evaluation of the nonglandular region of the stomach was undertaken, and a record of any lesions made using the EGUS Council severity scoring system (0e4/4) [2]. Animals included in the study (Grade 2e4/4 Ulcers) were paired initially according to their grade of ESGD lesion and were as similar as possible in their workloads and management. Workloads were grouped as follows: rest to light: horse only walking and trotting; light to moderate: up to 1 hour of work per day with competitions not more than 2 weekends per month, for example, racehorses not racing but in fitness work, those competing in show jumping and horseball; hard work: racehorses in active racing with fast work done at least twice a week. Where pairs could not be found within the exact workload grouping, the closest match to their individual exercise load was found (n ¼ 2). The horse identification numbers were individually listed on sheets of paper, which were then shuffled and then alternatively chosen to be put into the change or no change group. The horses allocated to the “change feed category” were all introduced onto the trial complementary feed. Horses that did not change diet continued with their usual feed, forage, and management. The trial complementary feed provided a similar estimated energy intake to their normal ration and was introduced over a 5e7 days acclimatization period. At one establishment, five horses in the change diet group also had their forage changed from straw only to meadow hay. All other horses in the change diet group remained on their prestudy forage. The protocol requested that all horses, regardless of whether or not the feed was changed, continued at their pretrial exercise level and maintained their competition schedule throughout the study. All owners reported similar work levels throughout the trial, except for 3 animals whose work levels varied due to issues unrelated to the study. All animals with ESGD Grades 3 and 4/4 were given the recommended dose of omeprazole (4 mg/kg per os once a day) for 4 weeks after which a repeat gastroscopic evaluation (Scope 2) was undertaken (within 24 hours of stopping the treatment). The horses then continued on their respective dietary regimens for a further 6 weeks at which point the final gastroscopic evaluation was made (Scope 3). Horses with ESGD Grade 2 lesions were not given any omeprazole but were still gastroscoped after 4 and 10 weeks. Any omeprazole dose was administered first thing in the morning before any forage or complementary feed had been given.
Body weight (BW) was estimated using a commercial heightspecific weight tape [6] before each gastroscopy. 2.2. Horses and Venues Ninety-nine horses (32 Thoroughbreds, 63 Warmblood sport horses, and four ponies; BW average 461 kg (range 277e600 kg), body condition score (BCS) median 5.5/9 (range 3e7/9) were initially scoped at four establishments, which for practical reasons were in close geographical proximity (within a 70 km area around Madrid), followed similar management practices, and fed (3 out of the 4 establishments) hay/haylage from the same source and supplier. The fourth establishment fed straw as the only forage. They were used for racing (n ¼ 26) and dressage (n ¼ 24) and show jumping (n ¼ 23) and horseball (n ¼ 26). Five horses had no evidence of any gastric lesions, one just had glandular ulcers, 17 had Grade 1 ulceration (17%), and 76 (77%) had ESGD ulcers Grades 2. For 10 of these 76 animals, an appropriate pair could not be found; therefore, 66 horses started the feeding study. A total of 58 (18 Thoroughbreds, 36 Warmblood sport horses, and four ponies; 12 aged between 2 and <4 years; 12 aged between 4 and <8 years; 32 aged between 8 and <14 years; and 2 animals aged >14 years) completed the whole protocol and participated fairly evenly across the four activities. The eight animals that did not complete the study were sold by their owners and left the area and were therefore lost to follow-up. Four came from the no change group and four from the change group, and two were already paired. The remaining horses were again primarily paired according to their gastric ulcer grade but also their workload and original diets. None of the horses had been studied or diagnosed as having any sort of ulcer before the study. 2.3. Management and Nutritional Information Key details of the training, management, and nutrition of the above horses before the start of the study were obtained. Their current digestible energy intake was estimated (based on manufacturer information or reference texts) and, for the horses that would be changing onto the trial complementary feed, an appropriate isocaloric intake from the study diet was determined. The trial complementary feed was a 50:50 mix of two proprietary complementary feeds (WINERGY Equilibrium Growth and SPILLERS HDF Power Cubes; MARS Horsecare UK Ltd) and was directed to be fed in three meals per day. Representative composite samples of the original diets (forage and complementary feeds) were sent for analysis by wet chemistry for starch, water-soluble carbohydrate (WSC), dry matter, and neutral detergent fiber (NDF) by Equi-Analytical of Dairy One. Nonstructural carbohydrate intake (NSC) was calculated as the starch plus WSC. 3. Statistical Analyses McNemar’s tests for all horses and each group (feed change or not) were performed using EGSD score of 2 or 3 as being clinically significant. McNemar’s tests were also used to identify changes in EGSD grade for both groups between Scopes 1 and 2; 1 and 3; 2 and 3 for horses initially graded as EGSD 2 (EM) and for horses initially graded as EGSD >2 (ES). Two different cut-offs at Grades 2 and 3 were used to dichotomize the ordinal ESGD scale. Normality tests were conducted on continuous data relating to original and trial diet composition and for weight data. Body condition score data were treated as if nonparametric. Wilcoxon sign rank or paired t-tests were conducted to identify differences in the dietary composition following a change in diet for those horses that
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
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Table 1 Starch, nonstructural carbohydrate (NSC), and neutral detergent fiber (NDF) intakes from the complementary feed only: mean (and range). Starch Content in Diet
Mean (Range), Starch g/kg, BW/d
Mean (Range), NSC g/kg, BW/d
Mean (Range), NDF g/kg, BW/d
Original diets for all horses Original diets for those horses that changed diet Following change in diet for those horses that changed diet
3.49 (0.48e6.37) 3.50 (0.77e5.98) 0.94 (0.33e1.55)
4.29 (0.97e7.72) 4.31 (1.29e7.31) 1.68 (0.60e2.78)
3.65 (1.01e8.05) 3.50 (1.19e7.53) 3.37 (1.21e5.58)
Abbreviation: BW, body weight.
changed diet. These analyses were performed for the trial diet alone and the trial diet and forage together. Wilcoxon sign rank or paired t-tests were also conducted to identify change in estimated BW and BCS in the two diet change or no diet change groups between Scopes 1 and 2, 1 and 3, and 2 and 3. Fisher exact tests were used to identify differences in any changes in behavior reported by owners in horses in each group (feed change or not). This analysis was performed separately for those horses that started the trial with an EGSD score of 2 and also for those horses that started the trial with an EGSD score of 3.
4.3. Nutrition
Fifty-five of the 58 animals maintained the same intensity and level of work throughout the study. However, one increased and two reduced their level of work for reasons unrelated to the study. Of the 29 horses that changed diet, 28 maintained the same workload, 0 increased and 1 reduced workload, and for those horses that did not change diet, 27 maintained the same workload and 1 increased and 1 reduced workload. The disciplines of the participant horses were also as evenly distributed as possible between the group that changed diets and the group that continued on the same diet. Nine racehorses, eight horseball horses, eight dressage horses, and four show jumpers had their diets changed to the study diet. The group that did not change diet consisted of seven racehorses, nine horseball horses, seven dressage horses, and six show jumpers.
At the start of the study, the nutritional intake from the complementary feeds being fed varied considerably as shown in Table 1. All horses received at least one commercial product, and for 33/58, the complementary feeds were provided twice a day, and the rest were fed three meals. For 17 (out of 29) animals that changed diet, the change in diet also meant an increase in the number of meals per day from two to three (all the others were already being fed their complementary feed ration in three meals). Meal timings otherwise remained consistent between the pairs throughout the study. None of the horses included in the study had access to pasture or paddock of any kind. Six different hays and one haylage were fed (mean intake 10.3gDM/kg BW/day; range 3.05e21.18) together with a variety of chaffs at the start of the study. The estimated dietary intake when combined with the complementary feed was as shown in Table 2 (ad libitum provision of forage was taken as providing 2% BW in dry matter. No allowance was made for any intake of any bedding. Any fiber-based balancer or chaff that was originally fed to the change in diet group was removed when they received the study diet. For one establishment, straw was fed as the only forage; therefore, for the five pairs based at this establishment, the change in diet also included changing to the hay provided by another study establishment. The core type of forage fed by each establishment remained the same over the study period, and any changes in forage batch fed were the same for each animal within a pair (i.e., same for those that had had their diet changed and those that did not). Whether examining the complementary feed alone or the complementary feed with forage, there were significant reductions in starch and NSC intake (P values < .001), but not NDF following the change of diet.
4.2. BW and BCS
4.4. Behavior
There was no significant change in estimated BW for those 58 animals that completed the study (455 ± 70; 447 ± 71; 443 ± 66 kg at the three gastroscopies, respectively) or between any of the scopes for either group of horses. In the group that did not change diet, there was a slight increase in BCS (median: 5e5.5; P value ¼ .04) between Scopes 2 and 3. In the group that did change diet, the median BCS at Scopes 1, 2, and 3 were 5.5, 5.5, and 5, respectively. There were statistically significant differences in all comparisons in BCS in this group for between Scopes 1 and 2 (P value ¼ .04), between Scope 1 and 3 (P value < .001), and between Scopes 2 and 3 (P value ¼ .006).
Initially, owners, riders, or trainers were asked if they felt their horse was healthy and how they felt about their horses’ physical appearance or behavior. Thirty-seven (64%) felt that their horses were healthy and made no comment; three owners said that they felt that their horses looked “poorly” with a lack of coat shine; six owners reported that their horses suffered occasional unexplainable colics; five reported that the horse was underweight; three commented that their horses suffered from fecal water syndrome; two reported the horses as “stressed”; one reported the horse as having a lack of appetite; one horse had been diagnosed with recurrent equine rhabdomyolysis, and another had been diagnosed
4. Results There were no clinical issues or other problems associated with the gastroscopies, and the DCs were well accepted in all 29 horses assigned to the “change diet” group. 4.1. Workload and Disciplines
Table 2 Starch, nonstructural carbohydrate (NSC), and neutral detergent fiber (NDF) intakes from the complementary feed and forage: mean (and range). Starch Content in Diet
Mean (Range), Starch g/kg, BW/d
Mean (Range), NSC g/kg, BW/d
Mean (Range), NDF g/kg, BW/d
Original diets for all horses Original diets for those horses that changed diet Following change in diet for those horses that changed diet
3.62 (0.93e6.41) 3.61 (0.93e6.02) 1.05 (0.49e1.94)
5.51 (2.90e8.23) 5.60 (3.20e8.23) 3.03 (1.42e5.36)
9.77 (3.69e16.72) 9.49 (3.69e16.21) 9.57 (4.89e22.9)
Abbreviation: BW, body weight.
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
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N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
with chronic piroplasmosis (although both of these horses were in full work and competing). At the second and third scoping, the owners were asked simply whether each individual horse had shown any change in their overall behavior or physical appearance and whether any such change was perceived as positive or negative. For the horses that started the trial with ESGD score of 2, there was a statistically significant difference in owner reported behavior change at the third scope when comparing a positive behavior change with negative or no change (P value ¼ .009). In this group, 8 of 12 horses on the trial diet had a positive behavior change, whereas only 1 of 12 horses that did not change diet was reported as having a positive behavior change. Other similar comparisons were not statistically significant. 4.5. Equine Squamous Gastric Disease Of the 58 animals that completed the study, at Scope 1, 24 had Grade 2 ulcers, 23 Grade 3 and 11 Grade 4 ulcers. One animal in the change diet group and one animal without a change in diet within the Grade3/4 ulcer group were not able to be scoped on the second occasion for competition reasons. Their data were removed for evaluating the efficacy of omeprazole and post omeprazole DC. As horses were paired based on the severity of ESGD score at the start of the study, there was no statistical difference in initial ESGD grade between the groups that undertook the DC or did not. 4.5.1. Looking at All Animals In both feed groups, there was a significant difference in ESGD score of 2 prevalence between Scopes 1 and 2 and between Scopes 1 and 3 (all P values < .001; Fig. 1). Regardless of feed change status, there was a significant reduction in the prevalence of ESGD score of 2 at Scopes 2 and 3 compared with at Scope 1. A difference between the two feed change groups was identified when comparing the change in ESGD score of 2 prevalence at Scopes 2 and 3: For those that changed diet: There was no significant difference in the prevalence of ESGD score of 2 prevalence at Scopes 2 and 3 (P value ¼ 1.0): 18 horses were ESGD 2 at Scope 2 AND <2 at Scope 3; three went from 2 to <2; three stayed at 2; four horses went from <2 to 2. For those that did not change diet: There was a significant difference in the prevalence of EGSD score of 2 prevalence at Scopes 2 and 3 (P value ¼ .027): 14 horses were EGSD <2 at
No diet change 4.5
Diet change
4 3.5
ESGD score
3 2.5 2 1.5 1 0.5 0 1
2
3
Scope number Fig. 1. Number of horses (represented by the size of the bubble) with each ESGD score at the start at each scoping for the two feed groups. An increase in the size of the bubble therefore reflects and increase number of animals at that score and vice versa.
Scope 2 AND <2 at Scope 3; one went from 2 to <2; three stayed as 2; 10 horses went from <2 to 2.
4.5.2. Grade 2 Ulcers Only For the 12 horses with Grade 2 ulcers that changed diet, there was a significant difference in ESGD score between Scopes 1 and 2 (P value ¼ .03) and Scopes 1 and 3 (P value ¼ .02). For the initial Grade 2 horses that did not change diet, there were also significant differences in ESGD score between Scopes 1 and 2 (P value ¼ .004) and Scopes 1 and 3 (P value ¼ .01). For neither group were there significant differences in EGSD score between Scopes 2 and 3 (P values ¼ .45 and .55, respectively). 4.5.3. Grade 3 and 4 Ulcers Only For the 17 pairs of horses with Grade 3 or 4 ulcers there was a significant effect of the omeprazole with all but one animal showing an improvement over the course of the treatment: three animals improved by 1 grade; 12 by 1.5e2 grades; 13 by 2.5e3 grades; and three by four grades with only one staying the same. Over the two groups, there was 81% good healing to a score of 0/1, with 13% moderate healing (to a score 2) and 6% showed no healing. For the no diet change group, there was a significant improvement from Scope 1 to Scope 2 (P < .001), but a significant worsening between Scopes 2 and 3 (P ¼ .005) and ultimately no significant difference from Scope 1 to 3 (P ¼ .08) that is no apparent long-term effect of the medical treatment. For the diet change group, there was a significant improvement from Scope 1 to Scope 2 (P < .001), and there was no significant difference between Scopes 2 and 3 (P ¼ .32), and there remained a significant difference from Scope 1 to 3 (P ¼ .003). This is illustrated in Fig. 2. At Scope 3, only three horses in the no diet change group were ESGD grade <2, whereas nine horses in the diet change group were ESGD grade <2. Of the five horses that had their complementary feed and forage changed, only two of them started with a Grade 3 ulcer, and both improved slightly following omeprazole. One of these animals continued to improve post cessation of treatment and one slightly worsened. 5. Discussion This, to the authors’ knowledge, is the first article to look at the effect of DC on the healing and recurrence of ESGD. The study confirmed that >80% of horses with Grade 3 or 4 ulcers responded well to omeprazole with respect to their ESGD with no additional positive or negative effect of DC. Six weeks after omeprazole treatment without DC, there was overall a worsening of gastric health so that, by the end of the trial, these animals overall were no different from the start (i.e., there was no long-term benefit of the omeprazole treatment). However, overall, those that changed diet remained significantly improved at the end of the trial suggesting an advantage of making these DCs. This would suggest that, especially when changes in management and training level are not feasible, making appropriate changes in the ration may be of value. There was no apparent effect of the change in diet on gastric ulceration in animals with ESGD Grade 2, although interestingly the owners or feeders subjectively reported some improvements in behavior [7], perhaps related to the reduction in starch or NSC intake. This was not reported with the higher grade ulcers, however, and suggests additional work is needed to explore this more fully. The response to omeprazole treatment was similar to that expected in the field [8]. The level of recurrence post omeprazole treatment was also as expected and confirms that dietary, training, or other environmental factors drive ulcer formation and that a
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
No diet change 4.5
Diet change
4 3.5
ESGD score
3 2.5 2 1.5 1 0.5 0 1
2
Scope number
3
Fig. 2. Number of horse (represented by the size of the bubble) at each scoping in the two diet groups that started with an ESGD score of 3 or 4/4. An increase in the size of the bubble therefore reflects and increase number of animals at that score and vice versa.
course of omeprazole acts, as expected, purely as a treatment, not as a long-term preventative agent. A range of different complementary feeds were provided to the animals at the start of the diet although many of the rations were based on manufactured feeds rather than home-mixed rations. A high proportion of the animals (17/29) that changed diet also had an increase in the number of meals per day (from two to three: all the others were already being fed their complementary feed ration in three meals), which may been additionally advantageous due to reduced starch intake per meal [4]. Further studies in larger numbers of animals would be needed to further tease out which specific changes in the ration are the main drivers of the benefit seen here. Forage provision remained the same within each pair as did the management and training as far as possible. For animals at three of the four establishments, the change in diet meant purely a change in the complementary component of the ration not the type or timing or amount of forage being provided. However, all these establishments were already feeding some form of hay or haylage. For one of the establishments, which was originally feeding straw, the change diet horses were also moved onto the same meadow hay that was being fed at two of the other establishments. This only affected five pairs of animals and for the five that changed their forage (as well as their complementary feed) only two had Grade 3 ulcers at the start, one of which continued to improve and the other regressed slightly; therefore, this did not apparently influence the overall results. Feeding predominantly straw as the forage has been shown to be a major nutritional risk factor to gastric ulcer formation [4], therefore, it seemed appropriate to make this change although it did not have any apparent effect on the results. The amount and timing of the forage were not changed at any establishment (as far as we know), and overall, the NDF intake did not change with the change in diet. Given the overall low-forage intake, it is therefore possible that even greater differences between the diet change and no diet change groups may have been seen if the forage component of the ration had also been further addressed (amount/timing) in the diet change group. The chosen study complementary feed diet is a ration that has been practically recommended for use in high-performance horses, and certainly, there was no effect on estimated BW. There was a slight decrease in body condition in the change diet group (compared with a slight increase in the no change group), suggesting perhaps some difference in the body composition in the two groups or reflecting the subjective nature of BCS especially around the 5e5.5/9 score. There were no reported adverse effects
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on performance despite the significant overall reduction in starch and NSC intake. Recent studies have suggested that forage-only diets can be used to meet the high energy requirements of horses in very heavy training [9], providing their energy provision is high enough, although questions over glycogen restoration persist. Key nutritional recommendations for reducing the risk of gastric ulceration are fundamentally based on studies comparing the diets of animals that do have and do not have ulcers and assessing the risk [4]. This is the first study to suggest that rations based on these principles (i.e., principally reduced starch or NSC intake per day and per meal) may be beneficial following medical treatment. Although the study diet provided overall significantly lowered starch intake per day and per meal (as can be seen from the original range of intakes); some animals with ulcers were already on a low daily starch intake of <1 g/kg BW per day, suggesting that although this aspect of the diet may play a role in ulcer formation, it is not the only potential causative agent. Also while a statistical difference with respect to Grade 3 or 4 lesions was shown between the responses of those with and without change in diet, the numbers were insufficient to explore whether the individual differences in response were associated with their initial diet or not. The study diet provided some other suggested nutritional components to reduce the risk of ulcer including a small amount of alfalfa chaff and additional oil [10], which may have also played a role. It has been suggested that calcium and protein, both high in alfalfa hay, buffer stomach contents, resulting in a protective effect on the squamous mucosa [3,11]. In contrast, recent work has suggested that certain forms of alfalfa chaff fed in very large amounts may increase the risk of EGGD perhaps due to mechanical damage [12,13]. As some alfalfa chaff was included in the study diet it was recorded as either yes or no at the start and end (with yes: taken as there being a significant lesion, with erosion or ulceration, of the glandular mucosa, and no: where there was no or only a minor change in the glandular mucosa with no visible pathology or erosion/ulceration), stating whether EGGD lesions were present that could potentially be considered to be of significance. Of those animals that completed the study and whose glandular region could be fully evaluated: 27 had some evidence of glandular lesions at the start, and 18 at the end of the study (10 with change in diet and 8 with no change). Six animals originally free from glandular ulcers had evidence of some glandular lesions by the end of trial (four on the changed diet and two on the no changed diet), whereas 22 animals negative for EGGD at the start were also negative at the end (11 with change in diet and 11 with no change). No firm conclusions can be drawn, other than there was no apparent noticeable adverse effect of the diet change on EGGD, especially as currently it is very difficult to assess EGGD over time with respect to severity, due to little correlation between endoscopic findings and histopathology [14]. In addition, the omeprazole was not given according to new recommendations for EGGD lesions [15,16]. This was a field trial, and while it may be more applicable to real life situations, it did mean that for logistical reasons the numbers of animals initially scoped was restricted to nearly 100. Although all but six did have evidence of ESGD, 17 only had lesions reported as Grade 1. Horses with such level of ulceration were not included as it was considered that it would be difficult to clearly define and show improvement or deterioration with such individuals. The relatively small numbers of animals (58) completing the whole study is an obvious limitation of this study. It is known for example that the workload is an important risk factor (2, 3) for ESGD, but there were not enough horses available in the area with the required ulcer score, the same discipline, and workload to form statistically significant discipline or workload groups. Obviously, the type of training and exercise will vary between racing and sporting horses; therefore, the groups were spread as evenly as possible primarily by
Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007
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N. Luthersson et al. / Journal of Equine Veterinary Science xxx (2019) 102742
ESGD score, then by workload and then as far as possible by discipline. In addition, by ensuring that the two animals within each pair were kept under similar management regimens as each other, it was hoped that other extrinsic potential EGUS risk factors would remain the same for those that changed diet and those that did not. However, this remains a limitation, and it is recommended that future work should evaluate further the relative efficacy of DC postmedical treatment cessation according to both discipline and workload.
6. Conclusions Despite the limitations and challenges related to field trials, this study is the first to provide evidence that appropriate DCs can be a beneficial management strategy for those with more severe ESGD. Further work is needed to evaluate the added benefits of improving forage provision.
Acknowledgments The authors thank the owners and their vets who trusted us with their wonderful horses and Christina Dominguez for helping us organize all the work at the Madrid racetrack. They also thank s, Dorka Fulop, vet students and apprentices, Manuel San Andre n, Atocha Calvo, and Maria Clara Colmenero, Alejandro Mercha Alonso, for tirelessly helping with so many aspects that needed to be handled to get this study done.
Financial disclosures n para Financial support for this study was provided by Fundacio la Promocion del Deporte Ecuestre, ScanVet Animal Health A/S, Norbrook Laboratories Limited, WALTHAM, and Mars Horsecare UK.
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Please cite this article as: Luthersson N et al., Effect of Changing Diet on Gastric Ulceration in Exercising Horses and Ponies After Cessation of Omeprazole Treatment, Journal of Equine Veterinary Science, https://doi.org/10.1016/j.jevs.2019.05.007