European College of Equine Internal Medicine Consensus Statement—Equine Gastric Ulcer Syndrome in Adult Horses

Abstract

The term Equine Gastric Ulcer Syndrome (EGUS) was first used in 1999 to describe gastric ulceration in the horse.1 However, as discussed by Merritt,2 the terminology is commonly misused. The committee reinforces the importance of distinguishing between diseases of the squamous and glandular mucosa because, as discussed in this statement, important differences exist between the two. In human medicine, the term peptic ulcer disease (PUD) is used as an umbrella term to describe erosive and ulcerative diseases of the stomach and it is recognized that a large number of individual diseases are present under the term.3 Furthermore, while some different diseases might share similarities in pathophysiology and treatment regimens, it is recognized in human medicine that the direct extrapolation of either from one specific disease (such as NSAID-associated ulceration) to another (such as Helicobacter pylori associated ulceration) is inappropriate.3 The committee recognizes that the terminology for EGUS requires clarification and proposes that the nomenclature be: Equine Gastric Ulcer Syndrome (EGUS) as a general all encompassing term to describe erosive and ulcerative diseases of the stomach consistent with the use of the term PUD in man; Equine Squamous Gastric Disease (ESGD) and Equine Glandular Gastric Disease (EGGD) as terms that more specifically describe the affected region anatomically. Within ESGD, both primary and secondary disease is recognized. Primary ESGD, the more common of the 2 forms, occurs in animals with an otherwise normal gastrointestinal tract. In contrast, secondary ESGD occurs in animals with delayed gastric outflow secondary to an underlying abnormality such as pyloric stenosis.4 The pathophysiology of EGGD remains to be elucidated and as such further subclassification of lesion type is not possible at this time. Instead, the committee recommends the use of descriptive terminology with a clear distinction of the anatomical region affected (cardia, fundus, antrum, or pylorus as shown in Figure 2) and the gross appearance of the lesion. The committee emphasizes that the affected region of the stomach should be clearly identified when communicating research and clinical findings. A summary of the proposed terminology is depicted in Figure 1. Recommendation: Expansion of the existing EGUS terminology to specifically identify squamous and glandular disease as ESGD and EGGD, respectively, as shown in Figure 1. The prevalence of gastric ulceration varies with breed, use, level of training, as well as between ESGD and EGGD. The highest prevalence of ESGD occurs in Thoroughbred racehorses with 37% of untrained horses affected, increasing to 80–100% within 2–3 months of race training.5-7 Standardbred racehorses have a similar overall ESGD prevalence of 44% that rises up to 87% in training,8-10 while 17–58% show/sport horses and 37–59% of pleasure horses are affected.11-15 Endurance horses have an ESGD prevalence of 48% during the out of competition period that rises to 66–93% during the competitive period, with lesions most prevalent in elite horses.16, 17 Horses that are rarely competed and predominantly used in their home environment have the lowest ESGD prevalence of 11%.18 The prevalence of EGGD is less well understood. Australian Thoroughbred racehorses have reported prevalences of between 47%6 and 65%.19 In endurance horses, the prevalence is 16% outside of the competition period and 27–33% while competing.16, 17 A retrospective study in the United Kingdom found EGGD in 54% of 191 leisure horses and in 64% of 493 sport horses.20 Comparably, 57% of horses used for a variety of purposes were reported to have EGGD in 2 separate studies.14, 21 The majority of EGGD lesions in all of the above studies were found within the pyloric antrum. A postmortem study of 3,715 horses over 72 years found significant associations between the presence of ulceration and breed (Thoroughbred and Standardbred breeds were more likely to have ulcers than cold-blooded horses) and sex (a higher prevalence was reported in stallions than mares and geldings).22 In contrast, 2 large cross-sectional studies of Thoroughbred racehorses documented no significant effect of age or sex on the likelihood of having ESGD.7, 23 Similarly, a large study in Standardbreds found no association between the presence of ESGD and age; however, there was an association between increasing age and worsening ulcer severity, the relative risk for which was greatest in geldings.8 In a retrospective study of 684 sport and leisure horses in the United Kingdom, no effect of age, sex or month of presentation was found on prevalence of ESGD or EGGD. However, a significant association was found between the Thoroughbred breed and the presence of ESGD in horses of any age.20 Together, these findings suggest that other factors such as intensity or duration of exercise outweigh any potential age or sex effect, but that a breed effect might be present with Thoroughbreds predisposed to ESGD. There are few large scale epidemiologic studies that investigated other risk factors for EGUS. Of those available, significant associations have been shown between ESGD and individual trainers, a metropolitan yard location (horses trained in urban areas were 3.9 × more likely to have gastric ulcers), a lack of direct contact with other horses, solid barriers instead of rails, and talk rather than music radio in the barn.23 Straw feeding and a lack of access to water in the paddock have been associated with an increased risk of EGUS in general.24 Further large scale work is required to better understand the epidemiologic factors which influence disease development, particularly EGGD which is largely unstudied at this point in time. Pasture turnout is considered to reduce the risk of EGUS although evidence supporting this belief if cnflicting. Horses with access to some turnout were less likely to have ESGD, and this risk was even lower if they were turned out with other horses in one study of Thoroughbred racehorses in training.23 Conversely no effect of quality of pasture, or time at pasture (stabled, stable and pasture, pastured) was shown on ESGD prevalence in another study of Thoroughbred racehorses.25 In addition, there were no differences observed on intragastric pH in horses fed ad libitum grass hay and grain twice a day (1 kg/100 kg/d) when they were housed in a grass paddock, in a stall on their own or in a stall with an adjacent companion, suggesting that pasture turnout on its own might not affect gastric pH per se.26 Similarly, free access to fibrous feed or frequent forage feeding is widely considered to reduce the risk of gastric ulceration although strong evidence supporting this belief if also lacking. Feeding alfalfa hay and grain results in higher gastric pH and less peptic injury to the gastric squamous mucosa than feeding brome grass hay or coastal Bermuda hay with no grain.27, 28 Furthermore, in a study evaluating the influence of a high fiber diet versus an iso-energetic low fiber diet both the number and severity of ESGD lesions was greater in the high fiber diet group.29 Together, these findings suggest that that the impact of forage feeding in the absence of other risk factor reduction might not be as great as previously believed. There is an increased likelihood of ESGD (severity score ≥2/5) when straw is the only forage provided24 suggesting that forage type might also be important. An increased time between forage meals (>6 hours between meals), compared with more frequent forage feeding (<6 hours between meals) increases the likelihood of ESGD.24 A more consistent effect is observed with increased starch/grain intake and this been associated with an increased risk of ESGD in animals working at various levels of intensity in a number of studies. There is a marked increase in ulceration when nonexercising animals are stabled and fed grain at 1% of BW, 1 hour before hay is fed.30 Similarly, exceeding 2 g/kg BW of starch intake per day is associated with an approximately 2-fold increase in the likelihood of ESGD grade ≥2/5.24 ESGD developed in all horses within 14 days of their removal from pasture, stabling (fed 6 kg concentrate feed/day) and entering a simulated training regimen.31 Intermittent access to water increases the risk of EGUS as it has been shown that horses without access to water in their paddock are more than 2.5 times more likely to have EGUS ≥ 2/5 than horses with constant access to water.24 This was the case for both ESGD or EGUS in all parts of the stomach. Fasting is a well described as a risk factor for ESGD and intermittent starvation causes and increases the severity of ESGD.32 Using this effect, an experimental model has been developed to produce ESGD; however, it is the opinion of the committee that the model's ability to replicate the multifactorial nature of clinical disease is limited. Recommendation: Given that the fasting model appears to poorly the multifactorial nature of gastric disease the committee that its use as an experimental model is not Instead, the committee recommends that or should on In the years of gastric ulcer the prevalence and severity of ESGD in horses with clinical and was to be greater than in horses without clinical Gastric ulcers have been associated with a of clinical in horses, a of strong evidence to these clinical or or an or or and There is some evidence to suggest that gastric ulcers are associated with an increased of in Gastric ulcers were reported in of horses with in one study of which to gastric ulceration as documented by a to There is an association between of and ESGD with of horses with ESGD over the of horses with ESGD in another study and horses that were a lower of ESGD than horses that been The for this is but might be horses are for of at an increased risk of the presence of ESGD might horses to gastrointestinal and have reported an association between or and gastric of in horses with gastric ulcers from to and might to as without it a clinical of gastric is associated with a high prevalence of gastric ulcers in racehorses in is as a clinical of gastric In a cross-sectional study in Thoroughbred horses, a association between gastric ulceration and was In contrast, other studies have to identify an association between and has been reported as a clinical of gastric ulceration in However, there is no evidence of a and it is and in the gastric ulceration is of a disease is a common that horses or are more likely to have and horses with a are more likely to have ESGD than are or normal In contrast, no effect of has been shown in and in in this might have an effect in There is an association between and ESGD, although the is The potential for EGUS to is of to few studies have investigated the potential between and the presence of EGUS. one of the clinical have an effect on for or in training, but the remains gastric ulcers in the absence of other clinical have an effect on The by which gastric ulceration might affect has not been but it has been proposed that might as a direct of gastric and in the squamous region of the stomach are similar to the lesions or disease which is common elite human with of of gastrointestinal during exercise that is to increasing exercise Furthermore, human with frequent have a time to compared to without there are only a few studies that have to an association between the presence of ulcers and in used as a of while used to exercise There is a significant association between the presence of ESGD and in Thoroughbred with associated with the presence of gastric of their severity or the number of Similarly, there is a significant association between the presence of ESGD and in Standardbred A case reported Thoroughbred racehorses that with and gastric ulceration as the only treatment with was The effect of ESGD, by intermittent feed to exercise has been of the study was with and no time to lower increase in specific and were found in horses, when compared to The for these differences is not clear but the that increased be and The committee that a of clinical might be present in individual of EGUS with of and the most prevalent at a on are not it is recognized that EGUS might in however, the factors that to other causes to be in clinical between ESGD versus EGGD are but Recommendation: a variety of clinical might be present in individual of they are and are poorly associated with the presence of EGUS. The committee not the of EGUS on clinical and recommends that EGUS be by as discussed The committee that is the only for gastric The has been described it is to the the pylorus and as lesions in these are There is no between the presence of ESGD and as such the presence or absence of one be used as for the presence or absence of the There are no or to in of gastric A has shown for of gastric but to the of the has not been reported in clinical to there is no association between the presence of gastric ulcers and the of either or treatment is common is not The committee the potential of treatment and the importance of distinguishing ESGD from EGGD, the of treatment without is not is that if treatment is and the to to treatment remains to out gastric disease as some animals not to of clinical of lesions has identified on of the severity of lesions is most commonly by a grade that the appearance at different A variety of different have been for the with from to A separate that lesion number and severity has also been In 1999 the Equine Gastric Ulcer proposed a to severity lesion and and that the should be for both clinical and research use, few of the have been for or for a number and severity, significant was found for the number of squamous this was compared with and it was found that it the number of squamous lesions while a scale A further study that the Equine Gastric Ulcer be as the EGUS of its of use, and the and of between this and the of the EGUS to their own This lack of between and the of clinical by different Recommendation: The committee recommends that the existing Equine Gastric Ulcer in be used for ESGD. There is on the of glandular The clinical of the different of glandular disease are to be well although there is in the appearance of glandular that also be in their appearance and in their Furthermore, separate of the and appearance is important in a better of glandular as might not to the normal appearance that squamous it appears that of severity and the appearance of the and mucosa might at it is not that these different be in a such as that used for ESGD. Recommendation: better the use of a for EGGD is not In the absence of a terminology the anatomical and appearance of lesions as in Figure 1 should be The the is rather than importance to individual has been that there is a between the severity of gastric ulceration and the severity of clinical and it is to that more lesions are more likely to in important The use of further more disease with higher However, this might not be or consistent and there is a of in the a direct between clinical and the severity, or location of gastric ulcers in Furthermore, that horses with EGUS not clinical and are considered to have or gastric these horses are without clinical or as there is treatment in some Furthermore, it has been that a of is required for clinical However, in of the glandular mucosa is considered to of the in results in of the and a similar effect is present in the is not but it appears that some horses with or to suggesting that such an effect might be present in a of the In contrast, some horses with disease not have clinical and to in to There is evidence to the that lesion grade with clinical this the committee that the of clinical should not be on appearance the should the of an lesions in of the its and clinical research on EGUS should on both clinical and A variety of factors to the of ESGD. of these factors share the common that they increase the of the squamous mucosa to In clearly that squamous are to and injury in a and time of the is by by the squamous of the in of of in concentrate not only and but also have been shown to with There is a between of squamous mucosa to and of the squamous mucosa results from the gastric up by the increased associated with than a with this racehorses have an increase in lesion severity and number of lesion within the squamous mucosa associated with increasing intensity of The severity of ESGD in high level endurance horses is to the of the In contrast, the pathophysiology of EGGD is poorly understood. The glandular mucosa from the squamous mucosa in that under normal it is to gastric with the pH in the of the stomach stable at between 1 and ESGD results from of mucosa to EGGD is to from a of the normal that the mucosa from gastric The factors that to of this are to be elucidated in the but in Helicobacter pylori and are the causes of gastric research in the has on these 2 there remains in the as to the of in EGGD. and might a in squamous but the is similar in the glandular mucosa is Furthermore, although such are present in ESGD their appears to be secondary as the to is have been identified in horses affected with EGGD in some other studies have to identify such The potential for to EGGD under clinical is An has been for and at higher than while at clinical and not gastric ulceration when for previously high prevalences of EGGD have been observed in with disease to the number of animals likely to under such on the evidence for as a is lacking. Similarly, although have the potential to EGGD in individual animals they are to be an important to the prevalence of disease at the to human medicine a large number of different diseases with separate in it is likely that different to the of EGGD in the The no is considered a of gastric ulcer in of the with it is the opinion that treatment is in the of both ESGD, for which its is well and EGGD, of the to identify an underlying as of and are the most commonly used of in the of which is the in the the that with to be before In contrast, work the on the and their is on of the is to in the treatment of in the opinion of the remains the of for treatment of EGUS. A variety of factors the and duration of treatment influence the of The of the is to in an of different the and of the of used to the in different is is and it is that some of is to of the within the environment of the and its a to this within a to the work has been on the relative of different of A study the of and 2 to as a not significant differences in Similarly, clinical study found no significant in the of an when compared with the In contrast, an has been shown to have approximately twice the of a of findings are in of of clinical studies. In a direct between no in was observed the used at 1 versus for the In another no in was between and of these findings suggest that lower of either or might be and The duration of required for of ESGD and EGGD has not been In of a pH above and for a of hours is required for of gastric ulceration and studies that of results in hours of however, the duration of at might be as as hours in some The results of clinical studies suggest even if the duration of is only this is for the treatment of ESGD as the treatment with from to is well In with this the are largely on the results of clinical and work while that further the duration of with a of and is has been well at its of for 28 days with ESGD of discussed the of lower but in the absence of specific evidence to lower the use of at appears when However, it is the opinion on the use of at 2 Similarly, on the reported clinical the use of at appears In the reduction in be at this time of the lack of on the use of these in a clinical The duration of treatment also studies have compared the of within the 28 day treatment period but an study that if of ESGD is to that it is by 21 a reduction in the treatment period for ESGD to appears of the or used it is important to at only approximately of ESGD lesions within a 28 day treatment and is before the of treatment to that has not to be in the treatment of ESGD but be considered as an when is not or has been shown to be has been shown to gastric in experimental and is most commonly used at for ESGD are in treatment for EGUS have not between squamous and glandular However, in a of studies only of EGGD lesions with days of treatment at in direct to an ESGD lesion of The for the of EGGD to treatment is not but factors the duration of with the duration of treatment required and the use of In the duration of treatment for glandular ulceration is on primary of the and the of treatment might be for EGGD. In and duration of treatment are required for and to be observed in The have observed in the majority of EGGD over a similar time however, it is recognized that clinical specifically this effect over time are lacking. An for the of EGGD to to is that might a in the or of glandular ulceration and that treatment might be discussed the of in the of EGGD is In ulceration in human of are observed with days of from are for the treatment of EGGD in the However, not of ulceration in Furthermore, no evidence to their use in the with a clinical no of the of over Recommendation: In with the for of and the of to be as a factor to EGGD and the absence of clinical supporting their use, it is the opinion that the use of in the treatment of EGGD is not their is the proposed of in the of EGGD, the use of as a of treatment is Furthermore, their use is not by as is the of is likely a of to of and all of which are likely to be in its use, a study reported a for EGGD of the pyloric at and at twice Further studies the of and the potential for between it and as reported in human medicine, are the above factors the for the treatment of EGGD the use of as for ESGD the of at twice as in Given the reported to this at appears is the opinion that a of of should be before are Further it is that in such further the underlying of such a appears before treatment is The to of ESGD is similar to should be on a case by case the greater the ability to impact on risk factors discussed the lower the for in the of and is used at for specific for the of EGGD have not been developed although the of as a for EGGD is with of horses worsening of their EGGD grade in a of treatment at from in the of treatment in the of associated ulceration has also been the time of the of for the of EGGD is however, its use as per the for ESGD is further are of their of use and have been and increase the in gastric studies to a effect in of ESGD, results from a case the of an a and has shown as a for both ESGD and Similarly, a feed of of in with might be in the of and a to have the of EGGD in a fasting model of to some however, their effect is and their use as a is not In the it is recognized as discussed strong evidence supporting some is lacking. the are on the of the and their opinion as to the Furthermore, to evidence for the of diet in EGGD and as such the are on risk factors identified for ESGD. the evidence supporting such a is access to quality grass pasture is considered or at frequent of hay might be a Horses fed hay should a of kg kg per horses and at risk of EGUS should a of high quality forage kg kg per that is and has low low forage is not a of high quality forage and straw a of might be a Straw should not be the only forage but be in the at kg kg Horses should be fed grain and as as Feeding of feed should be as a large of be if greater than 1 to 2 kg of feed is fed per and be to to The diet should not 2 g/kg of starch intake per day or more than 1 g/kg of starch per meals should not be fed less than 6 hours such as might reduce the risk of EGGD. with gastric fed by lower gastric and increased in their gastric compared to the evaluating the use of in the of EGGD are to if these are should be An increased risk of ESGD has been shown with or but not when were in feed or in lower in such the committee the use of with feed to be of The of this have from the in the of research or the of this by supporting a of the in during of the any direct or in the of the and the the of the no use of