Equine gastric ulcer syndrome is the general term used to describe ulcers of any part of the epithelial tissue of the stomach. In recent years, the Equine Gastric Ulcer Council has promoted the sub-division of equine gastric ulcer syndrome into two categories which more accurately describe where the ulcers occur. The first describes ulceration of the non-glandular, upper part of the stomach and is called equine squamous gastric disease. The second describes ulceration occurring in the lower glandular part of the stomach and is termed equine glandular gastric disease (Sykes et al, 2015). Ulceration has also been known to occur at the end of the oesophagus and in the upper regions of the duodenum (Andrews et al, 1999). The consensus statement on equine gastric ulcer syndrome further divided equine squamous gastric disease into primary disease, which occurs in horses with an otherwise normal gastrointestinal tract, and secondary disease which occurs in horses with pyloric stenosis (Sykes et al, 2015). At present, equine glandular gastric disease is less well categorised and simply reflects the region where it occurs in the stomach (van den Boom, 2022).
Equine squamous gastric disease is categorised using a scoring system recommended by the Equine Gastric Ulcer Council with a range of 0–4. The scoring is based on lesion number, size and depth of any lesions (Table 1). Currently, there are little data available on equine gastric glandular disease, so grading is not yet standardised. Until this condition is better understood, a specific hierarchical scoring system is not recommended. Instead veterinarians are encouraged to describe ulcer presence or absence, their appearance and where they are located.
Table 1. Scoring system recommended by the Equine Gastric Ulcer Council when describing ulceration of the non-granular mucosa of the equid stomach
| Score | Description of the squamous mucosa |
|---|---|
| 0 | The epithelium is intact and there is no appearance of hyperkeratosis |
| 1 | The mucosa is intact, but there are areas of hyperkeratosis |
| 2 | Small, single or multifocal lesions |
| 3 | Large, single or extensive superficial lesions |
| 4 | Extensive lesions with areas of apparent deep ulceration |
Adapted from Sykes et al (2015)
Incidence of equine gastric ulcer syndrome
Although 22% of feral horse populations experience gastric ulcer syndrome (Ward et al, 2015), the incidence is higher in the domesticated population (Table 2). This is primarily as a result of management and feeding cereal-based concentrates. Diagnosing equine gastric ulcer syndrome was problematic until the arrival of the 2 m gastroscope, with research commencing only in 1989 (Murray et al, 1989). Further gastroscopy developments have now described ulceration in all regions of the stomach and it is generally accepted that equine squamous gastric disease is high in most equine disciplines.
Table 2. The incidence of equine squamous gastric disease in horses in different disciplines in the UK
| % of population | Discipline |
|---|---|
| 80–100 | Thoroughbred racehorses in training*† |
| 87 | Standardbred trottersठ|
| 66–93 | Endurance‡§ |
| 17–58 | Show and sports horses||¶** |
| 37–59 | Leisure*||¶ |
| 11 | At home leisure†† |
Recent work has demonstrated that equine gastric glandular disease is also present in both feral and domesticated horse populations. Ward et al (2015) found equine gastric glandular disease at a rate of 30% in feral horse populations, while others have reported incidence in domesticated horses of 35–72% across different equine disciplines and populations (Luthersson et al, 2009; Sykes et al, 2015; Luthersson et al, 2019).
Causes of equine gastric glandular disease
The causes of equine gastric glandular disease are yet to be fully elucidated. Currently, failure of the normal gastric glandular mucosal defence mechanisms is thought to be the major cause (Sykes et al, 2015). Several studies have implicated stress (Scheidegger et al, 2017; Sykes et al, 2019) but it is not yet known if there is any link to feeding. Further details on equine gastric glandular disease can be found in van den Boom (2022) and Rendle et al (2018).
Dietary risk factors for equine squamous gastric disease
Essentially, equine squamous gastric disease occurs because the squamous mucosa is exposed to acid which erodes the surface, causing ulceration. Two acids are implicated: hydrochloric acid, which is continually secreted from the glandular mucosal gastric pits (Luthersson and Nadeau, 2013) and plays an essential role in protein digestion and pathogen control in the stomach; and lactic acid and volatile fatty acids, which come directly from fermentation and are the end products of microbial degradation (Andrews et al, 2017). The production of lactic acid and volatile fatty acids in the stomach should be relatively limited if the horse is fed as its digestive anatomy dictates (ie trickle fed high amounts of slowly degraded fibrous feedstuffs). Trickle feeding prevents over-filling of the stomach and maintains the flow of digesta into the small intestine. Mean retention time of feed in the stomach and small intestine should be quite short (2–3 hours; Chaucheyras-Durand et al, 2022), resulting in limited time for significant fermentation to occur, thus acid accumulation in the stomach should not be an issue.
Poor dietary choices and feeding management, such as meal feeding high-starch and/or high-sugar diets can initiate undesirable rapid fermentation and slow stomach emptying. Such a situation leads to high lactic acid and volatile fatty acid production, which can induce equine gastric ulcer syndrome (Murray and Schusser, 1993; Jonsson and Egenvall, 2006; Luthersson et al, 2009; Andrews et al, 2017).
The potential for stomach bacteria to produce lactic acid and volatile fatty acids is well documented. Julliand and Grimm (2016) reported that concentrations of the anaerobic bacteria and lactate utilisers, known degraders of starch, can reach up to 10 million colony-forming units per millilitre of stomach contents, producing 8 mmol/L of acid after a meal. Although this capacity for fermentation in the stomach can be activated, it is important to emphasise that high-starch and/or sugar, low-fibre diets are neither necessary nor desirable and will be detrimental to gastric health and overall wellbeing.
The other situations that increase mucosa–acid interaction, are when the diet is low in fibre or when the stomach is empty. Murray and Schusser (1993) reported that stomach pH in horses continually fed Timothy hay was 3.1, while those that were fasted had a pH of 1.5. Meal-feeding cereal-based diets can often result in periods when the stomach is empty, thus inadvertently increasing acid contact with the mucosa. Periods of 6 hours or more between feeds is associated with equine gastric ulcer syndrome (Luthersson et al, 2009). Further-more, low-fibre diets which often accompany high-starch/high-sugar diets, lack the necessary fibre to form a ‘fibre mat’ on top of the digesta which can help to reduce acid splash during exercise (Lorenzo-Figueras and Merritt, 2002).
Alfalfa hay or chaff is alkaline in nature, contains ulcer-protective ingredients such as calcium and protein, and has been shown by Bäuerlein et al (2020) to be ulcer-reducing in adult horses. However, a study by Fedtke et al (2015) cast doubt on the suitability of alfalfa chaff as a fibre feed for newly-weaned foals. In the study, newly-weaned foals fed chaff had an increased ulceration score post diet, particularly around the pylorus region of the stomach, compared with those fed hay. Newly-weaned foals are known to exhibit significant levels of squamous gastric disease, and all foals in this study showed increased squamous gastric disease after weaning. However, the foals in this study fed 3 times per day with either molassed or unmolassed alfalfa mixed in with 0.9 kg oats (ie 2.7 kg oats per day) had significantly more lesions compared with those fed 2.7 kg oats in 2 or 3 meals per day plus ad libitum hay. The authors attributed the increased lesions to the rough nature of the alfalfa stalks, which caused an abrasive action to an already compromised organ. This may have been the case, but it is just as likely that the foals chewed the chaff extensively, creating small particle size (which can be ulcer-promoting) which, when mixed with oats, created ideal conditions for ulceration. Furthermore, the difference in the hay compared to alfalfa chaff groups could be attributed to the trickle-feeding nature of the hay diet, which may have had a less detrimental effect on gastric health than the meal feeding of the alfalfa chaff.
Equine squamous gastric disease is highly prevalent in weaned foals, and sympathetic feeding during weaning should be the aim to avoid extending the duration or severity of squamous gastric disease. Modifications such as short-term reduction in cereal feeding and taking particular note of constant access to fibre and promoting chewing will help to promote a speedy recovery from post-weaning equine squamous gastric disease. If owners are concerned about feeding alfalfa chaff to foals, the benefits from this feed can still be gained by feeding alfalfa pellets (Vondran et al, 2016). These could be used as a full or partial replacement for cereals immediately after weaning until improvement in squamous gastric disease scores are seen.
High amounts of straw fed to adult horses can also have this physical effect in the stomach. Luthersson et al (2009) reported a 4.5-fold increase in mucosal ulceration when straw was fed as the sole forage. Straw in limited amounts (0.25 kg dry matter/100 kg bodyweight) can be a useful ‘filler’ for overweight horses, but its low nutritional content and limited fermentation in the hind gut can predispose to impaction colic, so its use should be limited.
There are several other widely accepted management-related predisposing factors for equine gastric ulcer syndrome, including: sudden changes in diet (Luthersson et al, 2009; Andrews et al, 2017), stress, electrolyte administration (Holbrook et al, 2005), fasting, starvation, administration of non-steroidal anti-inflammatory drugs (Fennell and Franklin, 2009) and restricting access to water (Luthersson et al, 2009), which increases the risk of developing gastric ulcers by 2.5 times. At present, unequivocal data to support an undisputed link of all of these with equine squamous gastric disease are lacking, and as such they may be stimulants for some horses but not for others.
There is clear evidence that keeping horses at pasture reduces, stress, stereotypic behaviours and allows expression of innate behaviours such as foraging (Mach et al, 2020). However, there is no evidence to support that this management system alone is an effective prevention strategy for gastric ulceration. Although the gastric pH of horses kept at pasture has been noted to be higher than when horses are stabled for long periods, if horses are trained and fed cereals while at pasture the incidence of gastric ulceration can still be high.
Symptoms and clinical signs
Symptoms of equine gastric ulcer syndrome are multifactorial, but only the following have a well-supported association with equine squamous gastric disease:
- Colic, where a reported association between squamous disease and colic was found in 83% of horses with recurrent episodes of colic (Murray et al, 1989; Vatistas et al, 1999; Dukti et al, 2006)
- Poor performance in Thoroughbred racehorses (Vatistas et al, 1999) and Standardbred racehorses (Jonsson and Egenvall, 2006) are associated with the presence of gastric ulcers, independent of their severity or the number of ulcers.
Other symptoms reported from a range of individual studies include: weight loss, poor appetite, poor coat, diarrhoea, girthing issues and reluctance to work.
While many of these might be caused by squamous gastric disease, there is a lack of data to support unequivocal association which makes them unreliable diagnostic tools. Crib biting, a common stereotypy has been linked with squamous gastric disease (Luthersson and Nadeau, 2013) but to date, few data have been gathered to link the onset of crib biting with squamous gastric disease. The presence of crib biting in horses is more likely because of stress associated with inappropriate management regimens, rather than the presence of ulcers per se (Daniels et al, 2019; Sykes et al, 2019). The suggestion that crib biting is performed to relieve stomach discomfort is highly tenuous. Crib biting does not increase saliva production (Houpt, 2012) so it is highly unlikely that stomach pain relief is the stimulation for this behaviour. If any relationship does exist, it is more likely that the action of crib biting stimulates the vagus nerve, which in turn stimulates gastrin production (from parietal cells), increasing gastric secretions.
Diagnosing equine squamous gastric disease
The only validated method of diagnosing equine squamous gastric disease is to perform gastroscopy (Andrews et al, 1999). However, gastros-copy is invasive and the horse needs to be starved for 12 hours before the procedure, which can be ulcer inducing in itself. Loss of mucosal integrity can be seen during gastroscopy, but grades given to lesions tend to be lower than grades given on necroscopy. Therefore, correlating lesion grade with clinical signs can be challenging (van den Boom, 2022). This makes linking symptoms to ulceration difficult, so veterinarians need to take account of gastroscope results, onset of clinical signs, individual horse activity and history when reaching a diagnosis.
An objective system of scoring some of the behavioural issues such as girthing behaviour, behaviour suggesting the horse is cold-backed and reluctance to work, alongside recording empirical data on weight loss and feed intake might help in the selection of more accurate indicative symptoms as diagnostic features for equine gastric ulcer syndrome.
Several non-invasive tests on the market have attempted to use parameters such as faecal albumin or haemoglobin as indicators of gastric ulceration, but no data has been reported to support their accuracy in diagnosing squamous gastric disease (Sykes et al, 2014).
Treatment of equine squamous gastric disease
As most squamous gastic disease will require veterinary intervention for initial healing, drug therapy that centres around reducing the mucosa–acid interaction is favoured. Omeprazole is the drug of choice as it has been proven to reduce acid secretion. The buffered or coated form of omeprazole, GastroGarda, at a dose of 4 mg/kg once daily for 28 days, consistently produces healing rates of 70–77% (Andrews et al, 1999).
While B vitamins, organic acids, sea-buckthorn berries and antacids have been shown to have effects, none are approved as veterinary medicines and so cannot be promoted as having properties that treat equine gastric ulcer syndrome or alleviate symptoms (van den Boom, 2022). Other ingredients such as magnesium hydroxide (a pectin-lecithin complex) and Saccharomyces cerevisae (brewers yeast) have also shown promise as prophylactic agents, but cannot be marketed as such.
Reducing the risk of equine squamous gastric disease
As poor feeding management is one of the major causes of squamous gastric disease, a good feeding regimen is the best way to prevent it. Appropriate feeding will depend on the activity and level the horse is performing at. However, in all cases, quality fibre should be the basis of the diet and other nutrient sources (fat and cereals) should only be added when energy demands are at a level that cannot be met by fibre alone. If diets are constructed with a strong base of quality fibre (a minimum of 1% bodyweight per day and preferably 1.5%), then behavioural needs will also be met and this should help to reduce general stress, as well as ulcer formation.
Although high-forage diets are strongly associated with low levels of squamous gastric disease, it is essential to note that feeding high levels of forage will not prevent it if high levels of cereals and sugars are also fed. Galinelli et al (2021) reported that horses fed diets that were higher than 1 g/kg bodyweight per meal of starch and sugar still presented with ulcers despite being fed >2% dry matter forage/kg of bodyweight per day. However, this study also demonstrated the importance of adequate forage in the diet, as out of a group of 48 horses (27 with squamous gastric disease and 21 controls), 21% of the horses with squamous gastric disease had inverted cereal:forage ratios, and 86% of that group had forage in-takes lower than 1.5% of bodyweight per day. Some of the horses (82% of clinical squamous gastric disease cases) were fed diets that contained more than 2 g of sugars and starch/kg of bodyweight per day, and in 41.5% of the diets, the sugar and starch provision was higher than 2 g/kg bodyweight per meal, which is well above current recommendation for diet formulations. The horses free of gastric ulcer syndrome were also fed an average of 3 meals per day (standard deviation ± 0.3), while the horses with gastric ulcer received only 2 meals per day, suggesting that feeding management plays a role.
As squamous gastric disease is present in feral horses, there will be horses that are fed high-forage/low-cereal diets that still present with squamous gastric disease. Galinelli et al (2021) reported that 17% of all horses that presented with gastric ulceration had sugar and starch intakes below 1 g/kg bodyweight per meal. This suggests that, for some horses, the main cause of squamous gastric disease was not diet formulation.
Conclusions
Equine squamous gastric disease is highly prevalent in the horse population and is associated with a range of negative welfare conditions such as colic, weight loss, poor appetite, girthing discomfort, poor coat and diarrhoea. Equine squamous gastric disease is best diagnosed using a combination of gastroscopy and case history, as other currently available tests are unreliable. The cause of the ulceration is acid erosion of the squamous epithelial tissue, so strategies to reduce the production and interaction of acid with the mucosa should be a priority when preventing and treating equine squamous gastric disease. While many management factors are postulated to play a role in ulcer formation, the main evidence-based initiators are meal-feeding high amounts of starch and sugar, underfeeding fibre and long periods without feed. To minimise equine squamous gastric disease, all horses should be fed 1.5% of their body weight in dry matter per day as fibre. When energy demands dictate that cereals are needed in the diet, they should be given in several small feeds over the course of the day, and water should always be available ad libitum both in the stable and at pasture.
KEY POINTS
- Provide continuous access to forage (grass or hay), ensuring a minimum intake of 1.5 kg dry matter/100 kg bodyweight per day. Add quality fibre to the ration before adding cereals and fat.
- When energy demands are too high to be met by forage alone, then feed cereals in small meals (4–6 times per day), providing no more than 1 g starch and sugar/kg bodyweight per meal.
- Supply water ad libitum.
- When managing overweight horses adding 0.25 kg of straw per 100 kg bodyweight can help to increase trickle feeding without adding extra energy to the diet.