EQUINE VETERINARY EDUCATION / AE / JANUARY 2017
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2009). The reason for the high prevalence of squamous ulcers is likely to be multifactorial. A previous study showed that exercising horses had increased abdominal pressure and decreased stomach volume, which resulted in low pH in the proximal stomach (Lorenzo-Figueras and Merritt 2002). Exercise allowed contraction of the stomach and reflux of acids from the ventral cardia onto the squamous mucosa, i.e. ‘acid splash’, leading to acid injury. In addition, it is typical for performance horses to be held off feed for variable times before exercise, thus decreasing gastric juice pH, and resulting in more liquid contents. A breakdown in the pH gradient in the stomach and less ‘mat like’ contents. This is likely to increase exposure of the squamous mucosa to acid (Murray 1994; Argenzio 1999). Furthermore, serum gastrin concentrations were shown to increase over time in exercising horses, which might contribute to increased gastric acid secretion in athletic horses (Furr et al. 1994).
Intermittent vs. continuous feeding Horses grazing at pasture have, in general, had a decreased prevalence of squamous ulcers (Murray et al. 1996; Murray and Eichorn 1996; Frank et al. 2005; Lester et al. 2007, 2008). However, recent studies have shown that the prevalence of squamous ulcer in horses exposed to pasture varies by regions and management (Bell et al. 2007; Husted et al. 2008). Grazing promotes a continuous flow of saliva and ingesta that buffer stomach acid (Murray and Schusser 1993). When feed is withheld from horses before racing or when stabled and fed intermittently, gastric pH drops rapidly and the squamous mucosa is exposed to an acid environment. Feeding forage in any form other than ad libitum increased the likelihood of squamous ulcers (grade ≥2/5) by 3.9 times (95% confidence interval = 1.5–10.4) in the study of Danish pleasure horses (Luthersson et al. 2009). In addition, a recent report showed that horses fed forage once daily were at a higher risk of developing squamous ulceration (EGUS score ≥2/4) than horses fed twice daily or more often (Pedersen et al. 2015). In contrast, a study showed that both pastured pregnant and non-pregnant mares had a high prevalence of squamous ulcers (Le Jeune et al. 2009). These horses were supplemented in the pasture with hay and cereal-based concentrates, which may have contributed to the high prevalence of squamous ulcers, as feeding grain is a risk factor. Alternatively, the high prevalence of squamous ulcers in these pastured mares might have been due to the horses consuming less forage during evening hours than during daytime hours, which may result in less saliva production and a low pH environment in the proximal stomach (Husted et al. 2008); a recent study by the same research group showed that proximal stomach pH was lower in the early morning hours (01.00–09.00 h) in horses housed on pasture. A recent study suggests that many stabled horses may finish an evening forage meal well before or close to midnight (Ellis et al. 2015) resulting in a prolonged period without forage which has been suggested to increase the risk of squamous ulcers (Luthersson et al. 2009). In addition, lack of water provision, when out on pasture, has been shown to increase the risk of squamous ulceration in horses (Luthersson et al. 2009).
Stall confinement and feeding practices Alongside feeding practices, stall confinement per se has been implicated as a risk factor for EGUS. A recent study,
however, showed that neither proximal nor ventral stomach pH changed significantly in horses housed in stalls alone, housed in stalls with a companion, or housed in a grass paddock (Husted et al. 2008). Therefore, other factors apart from diet, such as behavioural and stress response might contribute to squamous and glandular ulcers in stalled horses (Malmkvist et al. 2012). In that study, the amount of starch (>2.7 g/kg or 1.5 kg/day) and paternal stallion influenced the risk of squamous ulcers only, whereas faecal cortisol was higher in those horses with glandular ulcers, indicating different mechanisms for squamous vs. glandular ulcer formation. In contrast, horses moved from pastures to individual nonenvironmentally controlled stalls where they could see other horses in the pasture, showed a significant improvement in squamous ulcer scores compared to when they were at pasture; however, spontaneous healing occurred in only 3/9 (33%) of horses (Woodward et al. 2014). Improvement in the squamous ulcer scores in these horses after 14 days of stall confinement, when fed hay (1.5% bodyweight) and grain (0.5% bodyweight), might have been due to the horses being accustomed to the open nonenvironmentally controlled stalls, individual feeding, lack of competition for feed, ability to see other horses in pasture and a better nutritional plane than when at pasture and fed round bales supplemented with a limited grain ration (Skipper 2007).
Diet type Starch content Size and composition of any complementary (nonforage) meal is thought to have a profound effect on risk for developing squamous ulcers. It has been demonstrated that feeding a diet containing 0.5 kg of grain based concentrates (40% nonstructural carbohydrates [NSC]) per 100 kg bodyweight, produced 20 mmol/l acetic acid concentration in the stomach up to 5 h after feeding (Nadeau et al. 2000) and this concentration of acetic acid led to uncoupling of sodium transport in the squamous mucosa in an in vitro Ussing system (Andrews et al. 2006). Furthermore, another study in horses showed that a high starch-low forage diet increased squamous gastric ulcer scores in the horses compared to horses on a low starch diet (Al Jassim et al. 2008). Another study suggested that feeding an estimated intake of >1g starch/kg bwt/meal resulted in a 2.4-fold increase risk for potential clinically significant squamous ulceration (≥2/5) (Luthersson et al.
2009). Furthermore, serum gastrin concentration was highest in horses fed a high-grain diet
(Sandin et al. 1998). These diets also help to produce a more fibrous mat composition of the stomach contents that might provide a physical barrier, whereas diets high in NSCs are typically ingested more quickly in horses with squamous ulcers (Malmkvist et al. 2012) with less saliva production and are fermented readily by resident bacteria, resulting in the production of VFA. In the presence of low stomach pH (<4), VFA are absorbed into the squamous cells, which results in cellular acidification and inhibition of cellular sodium transport, cell swelling and acid injury (Nadeau et al. 2003a, b; Andrews et al. 2006). Sodium transport was downregulated in the squamous mucosa of young horses (age ≤5 years) when exposed in vitro to VFAs, compared to older horses (age ≥12 years) (Peretich et al. 2009). The inability of the squamous mucosa to transport sodium efficiently might predispose them to squamous ulceration, especially if high
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