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Colic Prevention to Avoid Colic Surgery: A Surgeon's Perspective
Journal of Equine Veterinary Science 76 (2019) 1e5
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Journal of Equine Veterinary Science journal homepage: www.j-evs.com
Review Article
Colic Prevention to Avoid Colic Surgery: A Surgeon's Perspective Anthony T. Blikslager* Department of Clinical Sciences, North Carolina State University, Raleigh, North Carolina
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 February 2019 Received in revised form 26 February 2019 Accepted 26 February 2019 Available online 6 March 2019
Management factors associated with colic, particularly related to stall confinement and nutrition, have been linked to alterations in gastrointestinal mucosal transport, motility, and microbiome, which in turn creates conditions that induce colic. In particular, meal feeding creates large changes in water movement in and out of the colon and alters the microbiome. These conditions may in turn result in colic conditions such as large colon impaction or large colon volvulus. In addition, a range of management and nutritional factors have been found to place horses at risk of select colic conditions such as ileal impaction. Other specific colic conditions, such as strangulating lipomas, may be related to fat metabolism in geldings and ponies, although the association with nutrition and the endocrine system are less well defined. It has long been understood that parasites are associated with colic, and with the advent of highly effective anthelmintics, parasite-induced colic has been markedly reduced. Nonetheless, equine mangers and veterinarians have to be aware of changes in parasite resistance or patterns of activity, such as the resurgence of large strongyles with surveillance-based management of parasites. Overall, understanding management risk factors can lead to recommendations that prevent colic in horses. Additional study of these factors may ultimately lead to reductions in the prevalence of colic by suggesting optimal management practices. © 2019 Elsevier Inc. All rights reserved.
Keywords: Forage Impaction Volvulus Lipoma
1. Introduction Colic is in large part a disease syndrome associated with management. Horses evolved on the North American plains as hindgut fermenters, grazing forage for up to 18 hours/day while constantly moving. Management of horses by people has changed this activity to include stall confinement and meal feeding, both of which alter the physiology of the gastrointestinal tract by altering motility and the microbiome. These changes are associated with certain forms of colic, such as large colon impaction. In addition, nutrition may result in specific forms of colic, such as strangulating lipomas. Furthermore, vigilance related to management of parasites is critical because changes in parasite prevalence or resistance results in select forms of colic. Specific changes in gastrointestinal physiology induced by changes in management, as well as specific forms of
Animal welfare/ethical statement: No animals were used as a part of this review article. In addition, this article has not been submitted to another journal, and no abstract of this work has been submitted. Conflict of interest statement: I have no conflicts of interest to declare. No funding was used to generate this review. * Corresponding author at: Anthony T. Blikslager, College of Veterinary Medicine, 1060 William Moore Drive, Raleigh, NC 27607. E-mail address: [email protected]. https://doi.org/10.1016/j.jevs.2019.02.023 0737-0806/© 2019 Elsevier Inc. All rights reserved.
colic related to changes in nutrition, exercise, and deworming programs are discussed, including how colic may be prevented. 2. Prevalence of Colic in Horses According to a US national survey conducted in 2001, approximately 4% of horses have an episode of colic annually, with a case fatality rate of 11% [1]. Strangulating obstruction, a disease process in which simultaneous occlusion of the intestinal lumen and vasculature results in ischemic mucosal injury, is arguably the principal cause of colic-associated deaths in horses. For example, a study conducted in the United Kingdom in a general equine practice setting over 2 years showed that 14 of 200 (7%) horses evaluated for colic died, and 12 of these 14 deaths were associated with intestinal strangulation [2]. However, approximately 40% of horses with colic that require surgical intervention are associated with simple obstruction of the gastrointestinal tract [3], including impactions and ingestion of foreign bodies. It is this group of surgical patients that have the greatest chance of being prevented by optimal management practices. These practices generally include feeding a diet based principally on forage (with concentrate added if needed for performance and/or adequate body weight), as well as turnout and exercise for > 12 hours/24 hour per day. Before assessing specific types of impaction colic, it is first important to understand the physiology of the equine gastrointestinal tract.
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3. Physiologically Critical Features of the Equine Digestive Tract Horses use the digestive strategy of hindgut fermentation, during which ingested forage is rapidly passed from the stomach along the small intestine (in excess of 20m in the average 500 kg adult horse, with a transit time of approximately 120e180 minutes) and into the cecum and large colon [4]. This may be less efficient than the digestive strategy of foregut fermentation, noted in ruminants, where forage that has been partially digested in the forestomaches can then enter the small intestine for efficient absorption of nutrients [5]. However, selection pressure for speed in horses to run from predators (top speed, approximately 70 km/h) likely resulted in development of a hindgut, where a large gut chamber would not impede running. The equine hindgut is voluminous and folded to accommodate its length within the abdomen into a double horse-shoe configuration with a ventral colon (the lower horse-shoe) primarily functioning as the fermentation chamber, and the dorsal colon (the upper horse-shoe) taking on a predominant role in water absorption [6]. The pelvic flexure, which connects the ventral and dorsal colons, comprises a hairpin turn from the larger diameter ventral colon to the smaller diameter dorsal colon. Suboptimal management of horses, such as feeding of poor quality forage, may lead to ingesta obstructions (impactions), which are most commonly found at the pelvic flexure [7]. Impactions of indigestible luminal contents, most notably sand, tend to obstruct at a more distal flexure present between the right dorsal colon and the transverse colon [8]. The rapid passage of digesta along the small intestinal tract requires relatively large volumes of fluid, which are primarily secreted by the salivary glands, pancreas, and small intestinal mucosa [4]. The relative fluid volumes entering the equine digestive tract have been studied, and show that horses secrete approximately one extracellular fluid volume (calculated as 30% of body weight, or 150L in a 450 kg horse) into the digestive tract on a daily basis [4,6]. Control of absorption of NaCl and associated water movement across the equine colon has been studied in depth at both the local and systemic levels [6,9e12]. The endocrine-gut axis is critical to maintaining homeostasis considering the massive shift of fluid into and back out of the colon that occurs during the feeding of a meal, and this is accomplished by activating the reninangiotensin-aldosterone system interacting with colonic mucosal transporters [9,10,12]. This system is maximally activated during feeding of meals, which occurs during intensive management of horses [6]. In response to a single meal comprising the full ration for a horse in the form of hay-grain pellets, plasma renin activity was increased by 0.5 hours, followed by elevations in plasma aldosterone by 3 hours. The renin release was attributed to transient hypovolemia, as suggested by increases in plasma protein and packed cell volume [11]. This systemic hypovolemia is a consequence of fluid moving into the digestive tract. Studies have also shown that an increase in aldosterone in the horse results in a doubling of Naþ absorption in the proximal colon (ventral and dorsal colons), and a tripling of Naþ absorption in the distal colon as a mechanism to retrieve the large volumes of fluid that are secreted into the digestive tract [12]. Therefore, meal feeding places horses at risk of conditions such as colonic impaction, as a result of dramatic shifts in colonic fluid, or colonic distension, which can lead to colonic displacement or volvulus. 4. Simple Obstruction Simple intestinal obstruction is a physical obstruction of the lumen without obstruction of mesenteric vascular flow. The most common causes are intraluminal masses composed of feed material
(e.g., ileal impaction) or accumulation of parasites (e.g., ascarid impactions). There are other instances in which the bowel is obstructed without associated compromise of blood supply, for example, by extraluminal compression by a mass or band of tissue in horses with intraabdominal adhesions. The large volume of fluid entering the small intestinal lumen on a daily basis [10,12] causes the obstructed intestine to become distended. 4.1. Ascarid Impactions Impactions caused by Parascaris equorum typically occur in weanling foals that have been on a poor deworming program and that are administered an anthelmintic when they have a heavy parasite burden [13]. Products that cause sudden ascarid paralysis or death, including piperazine, organophosphates, and pyrantel pamoate, have been incriminated. However, it is likely that any effective broad-spectrum anthelmintic, such as the avermectins or moxidectin, will have the same effect. The lifecycle of Parascaris equorum includes ingestion of eggs from the pasture, migration into the lungs, and swallowing of larvae following coughing. Once in the intestine, the adult ascarids attain a length of up to 50 cm [13]. Therefore, it is critical to begin deworming foals at 4e6 weeks of age to prevent maturation of these parasites. In addition, there have been reported regional patterns of resistance to anthelmintics such as ivermectin [14], so that deworming programs require specific knowledge of which anthelmintics to use to reduce parasite burden while avoiding resistance. 4.2. Ileal Impaction Ileal impactions occur almost exclusively in adult horses in the southeastern United States. Although feeding of coastal Bermuda hay has been implicated in the regional distribution of this disease, it has been difficult to separate geographic location from regional hay sources as risk factors. However, a study from the southeastern United States showed that feeding coastal Bermuda hay and failing to deworm with an anthelmintic with efficacy against tapeworms are significant risk factors for ileal impaction [15]. Furthermore, in a study performed in the United Kingdom, horses with evidence of tapeworm (Anoplocephala perfoliata) infection were at risk for developing ileal impaction [16]. The latter likely results from an accumulation of mature tapeworms at the ileocecal junction. Tapeworms are difficult to surveil because the eggs rarely appear in a routine fecal flotation, although there is a serum test to test for antibodies to Anoplocephala perfoliate [16,17]. Routine deworming at least once annually for tapeworms is recommended. As far as the role of coastal Bermuda hay in ileal impactions, the precise reasons why it is associated with ileal impaction are unknown. However, it is a finer grass than other grasses, and there is the likelihood that when harvested for hay, an increased fiber level results in fine soft fibers that may be improperly chewed. The fibers then get caught in the ileocecal junction, ultimately blocking the passage of ingesta. The level of acid detergent fiber (ADF) or neutral detergent fiber (NDF) on a hay analysis that a horse can withstand is unknown because it likely also depends on individual horse factors such as dentition and familiarity with coastal Bermuda hay. Therefore, careful management practices include slow introduction of coastal Bermuda hay to horses that are not accustomed to this forage type, and use of the best quality coastal Bermuda hay because there is likely less room for error, as compared to other coarser grass hays. Hay quality can be related to digestibility, which is typically derived from in vivo trials. However, mathematical modeling has been used to derive dry matter digestibility (DMD) for horses from hay analyses, with the best models relating DMD to NDF and crude protein [18].
A.T. Blikslager / Journal of Equine Veterinary Science 76 (2019) 1e5
4.3. Large Colon Impaction Impactions of the large colon with ingesta occur at sites of anatomic reductions in luminal diameter, particularly the pelvic flexure and the right dorsal colon [19]. Although there are a number of reported risk factors, most have not been proven. However, a sudden restriction in exercise associated with musculoskeletal injury appears to be frequently associated with onset of impaction. In addition, one study evaluating 120 horses with large colon impaction showed that 41% of cases were diagnosed in the winter [20], possibly related to reduced water intake or changes in diet. Equine feeding regimens may be very important in the development of large colon impactions. For example, twice-daily feeding of concentrate is associated with secretion of large volumes of fluid into the small intestine, resulting in transient hypovolemia (15% loss of plasma volume) [6]. This leads to activation of the reninangiotensin-aldosterone system, and because aldosterone stimulates absorption of fluid from the large colon, this may dehydrate colonic contents [6,12]. Large concentrate meals may decrease small intestinal transit time, resulting in increased presentation of soluble carbohydrate to the cecum and large colon. Large shifts of fluid into the colon occur as concentrates are readily fermented in the large intestine, which would be expected to activate the reninangiotensin-aldosterone system. This in turn triggers net fluid absorption from the large colon. The effects of these large fluid fluxes on development of large intestinal disorders remain to be fully characterized, but almost undoubtedly, they play some role in the syndrome of colic. From a practical standpoint, intestinal fluid fluxes may be reduced with frequent small feedings (dividing the ration into up to 6 equal portions) in those horses requiring concentrate to maintain condition [6,11]. In addition, presentation of soluble carbohydrate can trigger large shifts in the microbiome [21], which may lead to clinical syndromes such as endotoxemia and laminitis with rapid proliferation and breakdown of gramnegative bacteria [22]. 4.4. Sand Impactions of the Large Colon Sand impaction of the large colon is common in horses with access to sandy soils, particularly horses whose feed is placed on the ground. Sand accumulates in the large colon, primarily the right dorsal colon, but may be present in multiple locations [8,23]. In addition, sand may trigger diarrhea, presumably as a result of irritation of the colonic mucosa [24]. Sand is typically found in the feces, most simply by adding water to several fecal balls in a palpation sleeve and hanging the sleeve. If there is sand, it will collect in the fingers of the sleeve. Although the amount of sand in the feces does not necessarily correlate with accumulation of sand in the colon, it is advisable for owners to consider methods to reduce sand ingestion or increase sand clearance. Administration of psyllium hydrophilic mucilloid in water by stomach tube in an experimental study in which sand was surgically placed in the colon did not show increased clearance of sand with psyllium [25], but in horses with natural accumulations of sand, psyllium (1 g/kg body weight) in combination with magnesium sulfate (1 g/kg body weight) did significantly reduce the volume of sand (based on radiographs) [26]. However, there is no evidence of significant clearance of sand when feeding psyllium at home [27]. Nonetheless, more study of psyllium is likely warranted based on extensive anecdotal evidence for its ability to reduce the prevalence of sand colic. 5. Colic Associated with Ischemia Horses with strangulating lesions have consistently higher mortality rates, including preoperative and operative mortality in
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which horses with a poor prognosis based on the level of systemic inflammatory response syndrome may be electively euthanized before surgery, or horses at surgery may be euthanized because of the extent of injury or anatomical location [28,29]. Horses with intestinal diseases other than strangulating obstruction may also suffer from ischemic disease. For example, horses suffering from simple obstruction ultimately succumb to ischemic necrosis if not attended to medically and sometimes surgically as increasing intraluminal pressure progressively occludes the circulation within the intestinal wall [30,31]. Although strangulating obstruction is generally considered to be an “act of god” with no means of prevention, there are instances where management techniques may reduce the incidence of strangulating obstruction. In particular, there are two disease states of note that may be preventable: small intestinal strangulation by pedunculated lipoma and large colon volvulus. 5.1. Strangulation by Mesenteric Pedunculated Lipoma Lipomas form between the leaves of the mesentery as horses age, and mesenteric stalks likely develop as the weight of the lipoma tugs on the mesentery. The stalk of the lipoma and a loop of the small intestine or small colon may become intertwined, causing strangulation. Mature or aged horses (typically > 15 years of age) are at risk of strangulating lipomas [32]. In addition, geldings and ponies are also at risk for developing strangulating lipomas [32,33], which raises the possibility of alterations in metabolism and diet as possible risk factors. Although there have been no studies to assess the role of nutrition or gender on mesenteric fat deposition, there has been a study correlating body condition score with internal fat deposition [34]. There were significant correlations between body condition score and retroperitoneal fat, but not mesenteric fat, suggesting differences in fat deposition. However, further studies are warranted, particularly in populations of horses used for pleasure and sport activities that may be on a more lipogenic diet rather than the horses going to slaughter, which have been studied to date [34]. Ultimately, it may be possible to reduce the prevalence of lipomas with diet or by management of endocrinopathies in geldings and ponies. 5.2. Large Colon Volvulus This is the most fatal form of colic, although a recent study has shown that early recognition and surgical correction of the condition can result in a good outcome [35]. However, experimentally, the colon is irreversibly damaged with 3e4 hours of 360-degree volvulus of the entire colon [36], so that most horses not within a short distance of a referral hospital succumb to the disease. This should heighten interest in prevention of the disease. Large colon volvulus is most prevalent in peripartum Thoroughbred broodmares, although these is inherent bias in studies primarily from Thoroughbred breeding regions such as Lexington Kentucky [35] and Ocala Florida [37]. However, studies from the United Kingdom have revealed that broodmares that have a history of foaling are at risk regardless of breed [38]. Other interesting findings from this same study included management risk factors, such as an increase in the hours of stabling in the days leading up to colic, an increasing number of horses on the farm, and 3 or more people involved in the horse's care [38]. These factors all suggest that increased confinement or changes in foraging patterns are associated with colonic colic. Interestingly, increases in stabling has been studied in particular and shown to alter colonic motility [39]. Variables related to nutrition associated with increased risk of large colon volvulus included being fed hay in the last 28 days, being fed sugar-beet in the last 28 days, and an alteration in the amount of
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forage fed in the last 7 days. These may relate to the practicalities of managing broodmares in the peripartum period but also suggest that alterations in forage or digestible fiber may result in microbiome changes favoring a change in motility, a change in gasproducing bacteria, or both, thereby triggering initial gas distension and displacement of the colon. 5.3. Thromboembolic Colic In another form of ischemic disease, horses may suffer from nonstrangulating infarction, which is most commonly associated with parasite migration [40]. Although thromboemboli have been implicated in the pathogenesis of this disease, careful dissection of naturally occurring lesions has not revealed the presence of thrombi at the site of intestinal infarctions in most cases, suggesting that vasospasm plays an important role in this disease [40]. Although this disease process has become relatively rare with the advent of effective broad-spectrum anthelmintics, there has been a notable increase in infection with Strongylus vulgaris, the principal parasite that triggers thromboembolic colic [41]. This has partly resulted from surveillance-based deworming programs, primarily aimed at small strongyles. Therefore, careful assessment of deworming programs continues to be a critical component of management to reduce the incidence of colic. 6. The Equine Microbiome There has been recent interest in the equine microbiome and how it is altered under differing management practices. Numerous differences have been described in the fecal microbiota of postpartum mares that preceded colic (defined as an episode of abdominal pain based on the mare's behavior [pawing and rolling] that lasted >2 hours and required administration of analgesics). For example, one study found associations between changes in Firmicutes and Proteobacteria, most notably Lachnospiraceae and Ruminococcaceae, and the development of colic [42]. Furthermore, the authors of this study suggested that select changes in the fecal microbiota could possibly be used to predict higher risk of colic [42]. Although studies on equine microbiota have often focused on fecal microbiota, it has been shown that fecal microbiota are not reliably indicative of colonic microbiota [43]. Nonetheless, another study evaluating the effect of concentrate diet on colonic microbiota collected at the time of slaughter has shown some similar results to the aforementioned fecal microbiota study. In particular, feeding of dietary concentrate (the core diet for all concentrate-fed horses consisted of a coarse mix balancer (2e2.5 kg/d; 20e25 kJ digestible energy/g), hay/haylage (6 kg/d; 60 kJ digestible energy/ g), and barley (1 kg/d; 13 kJ digestible energy/g)) resulted in a significant increase in Lachnospiraceae [44]. This same study showed that horses fed concentrate diet (listed above) versus a grass-only diet had an increase in lactic acid-producing microbiota (the BacilluseLactobacilluseStreptococcus group) in their colonic contents (obtained following euthanasia), resulting in higher concentrations of lactic acid. Interestingly, the shift to lactic acidproducing microbiota was also associated with horses that developed colonic distension or impaction [44]. Despite changes that appear to be selective enough to be used to detect horses at risk of colic, a great deal of variability in individual horse microbiota even when managed under similar circumstances has been shown [43], suggesting caution when interpreting microbiome-related risk factors in individual or small groups of horses. Furthermore, with the number of different “concentrate” diets now available, including high-fat diets, and diets containing fiber, versus a pure grain concentrate diet, dietary factors would have to be assessed accurately as to which microbiome changes they may induce.
7. Conclusions When evaluating the evidence assessing the link between management and dietary factors and their association with colic, it is becoming increasingly clear that practices such as meal feeding and stalling of horses for the majority of the day (>12 hours) causes notable physiological changes, including changes in mucosal water transport [10], that can result in diseases as severe as large colon volvulus. Continued efforts to further evaluate the effects of equine management on the microbiome will likely provide more clues as to the pathogenesis of colic and a greater ability to institute preventive measures. These measures should continue to include simple techniques such as continuous access to forage and consistent daily exercise but continued provision of more specific advice related to deworming programs and the optimal diet to minimize daily fluctuations in colonic fluid flux and shifts in the microbiome should be provided to owners in an attempt to reduce the prevalence of colic. References [1] Traub-Dargatz JL, Kopral CA, Seitzinger AH, Garber LP, Forde K, White NA. Estimate of the national incidence of and operation-level risk factors for colic among horses in the United States, spring 1998 to spring 1999. J Am Vet Med Assoc 2001;219:67e71. [2] Proudman CJ. A two year, prospective survey of equine colic in general practice. Equine Vet J 1992;24:90e3. [3] Mair TS, Smith LJ. Survival and complication rates in 300 horses undergoing surgical treatment of colic. Part 1: short-term survival following a single laparotomy. Equine Vet J 2005;37:296e302. [4] Argenzio R. Physiology of digestive, secretory, and absorptive processes. In: White NA, editor. The equine acute abdomen. 1st ed. Philadelphia: Lea & Febiger; 1990. p. 25. [5] Janis C. The evolutionary strategy of the equidae and the origins of rumen and cecal digestion. Evolution 1976;30:757e74. [6] Clarke LL, Roberts MC, Argenzio RA. Feeding and digestive problems in horses. Physiologic responses to a concentrated meal. Vet Clin North Am Equine Pract 1990;6:433e50. [7] Dabareiner RM, White NA. Large colon impaction in horses: 147 cases (19851991). J Am Vet Med Assoc 1995;206:679e85. [8] Ragle CA, Meagher DM, Lacroix CA, Honnas CM. Surgical treatment of sand colic. Results in 40 horses. Vet Surg 1989;18:48e51. [9] Clarke LL, Argenzio RA. NaCl transport across equine proximal colon and the effect of endogenous prostanoids. Am J Physiol 1990;259:G62e9. [10] Clarke LL, Argenzio RA, Roberts MC. Effect of meal feeding on plasma volume and urinary electrolyte clearance in ponies. Am J Vet Res 1990;51:571e6. [11] Clarke LL, Ganjam VK, Fichtenbaum B, Hatfield D, Garner HE. Effect of feeding on renin-angiotensin-aldosterone system of the horse. Am J Physiol 1988;254:R524e30. [12] Clarke LL, Roberts MC, Grubb BR, Argenzio RA. Short-term effect of aldosterone on Na-Cl transport across equine colon. Am J Physiol 1992;262:R939e46. [13] Cribb NC, Cote NM, Boure LP, Peregrine AS. Acute small intestinal obstruction associated with Parascaris equorum infection in young horses: 25 cases (1985-2004). N Z Vet J 2006;54:338e43. [14] Lyons ET, Tolliver SC, Collins SS. Prevalence of large endoparasites at necropsy in horses infected with Population B small strongyles in a herd established in Kentucky in 1966. Parasitol Res 2006;99:114e8. [15] Little D, Blikslager AT. Factors associated with development of ileal impaction in horses with surgical colic: 78 cases (1986-2000). Equine Vet J 2002;34: 464e8. [16] Proudman CJ, French NP, Trees AJ. Tapeworm infection is a significant risk factor for spasmodic colic and ileal impaction colic in the horse. Equine Vet J 1998;30:194e9. [17] Barrett EJ, Farlam J, Proudman CJ. Field trial of the efficacy of a combination of ivermectin and praziquantel in horses infected with roundworms and tapeworms. Vet Rec 2004;154:323e5. [18] Hansen TL, Lawrence LM. Composition factors predicting forage digestibility by horses. J Equine Vet Sci 2017;58:97e102. [19] White 2nd NA, Dabareiner RM. Treatment of impaction colics. Vet Clin North Am Equine Pract 1997;13:243e59. [20] Jennings K, Curtis L, Burford J, Freeman S. Prospective survey of veterinary practitioners' primary assessment of equine colic: clinical features, diagnoses, and treatment of 120 cases of large colon impaction. BMC Vet Res 2014;10(suppl 1):S2. [21] Warzecha CM, Coverdale JA, Janecka JE, Leatherwood JL, Pinchak WE, Wickersham TA, et al. Influence of short-term dietary starch inclusion on the equine cecal microbiome. J Anim Sci 2017;95:5077e90.
A.T. Blikslager / Journal of Equine Veterinary Science 76 (2019) 1e5 [22] Sprouse RF, Garner HE, Green EM. Plasma endotoxin levels in horses subjected to carbohydrate induced laminitis. Equine Vet J 1987;19:25e8. [23] Kilcoyne I, Dechant JE, Spier SJ, Spriet M, Nieto JE. Clinical findings and management of 153 horses with large colon sand accumulations. Vet Surg 2017;46:860e7. [24] Bertone JJ, Traub-Dargatz JL, Wrigley RW, Bennett DG, Williams RJ. Diarrhea associated with sand in the gastrointestinal tract of horses. J Am Vet Med Assoc 1988;193:1409e12. [25] Hammock PD, Freeman DE, Baker GJ. Failure of psyllium mucilloid to hasten evaluation of sand from the equine large intestine. Vet Surg 1998;27:547e54. [26] Niinisto KE, Ruohoniemi MO, Freccero F, Raekallio MR. Investigation of the treatment of sand accumulations in the equine large colon with psyllium and magnesium sulphate. Vet J 2018;238:22e6. [27] Kaikkonen R, Niinisto K, Lindholm T, Raekallio M. Comparison of psyllium feeding at home and nasogastric intubation of psyllium and magnesium sulfate in the hospital as a treatment for naturally occurring colonic sand (geosediment) accumulations in horses: a retrospective study. Acta Vet Scand 2016;58:73. [28] Proudman CJ, Smith JE, Edwards GB, French NP. Long-term survival of equine surgical colic cases. Part 2: modelling postoperative survival. Equine Vet J 2002;34:438e43. [29] Proudman CJ, Smith JE, Edwards GB, French NP. Long-term survival of equine surgical colic cases. Part 1: patterns of mortality and morbidity. Equine Vet J 2002;34:432e7. [30] Allen Jr D, White 2nd NA, Tyler DE. Morphologic effects of experimental distention of equine small intestine. Vet Surg 1988;17:10e4. [31] Dabareiner RM, Sullins KE, Snyder JR, White 2nd NA, Gardner IA. Evaluation of the microcirculation of the equine small intestine after intraluminal distention and subsequent decompression. Am J Vet Res 1993;54:1673e82. [32] Blikslager AT, Bowman KF, Haven ML, Tate Jr LP, Bristol DG. Pedunculated lipomas as a cause of intestinal obstruction in horses: 17 cases (1983-1990). J Am Vet Med Assoc 1992;201:1249e52. [33] Garcia-Seco E, Wilson DA, Kramer J, Keegan KG, Branson KR, Johnson PJ, et al. Prevalence and risk factors associated with outcome of surgical removal of pedunculated lipomas in horses: 102 cases (1987-2002). J Am Vet Med Assoc 2005;226:1529e37.
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[34] Morrison PK, Harris PA, Maltin CA, Grove-White D, Argo CM. EQUIFAT: a novel scoring system for the semi-quantitative evaluation of regional adipose tissues in Equidae. PLoS One 2017;12:e0173753. [35] Hackett ES, Embertson RM, Hopper SA, Woodie JB, Ruggles AJ. Duration of disease influences survival to discharge of Thoroughbred mares with surgically treated large colon volvulus. Equine Vet J 2015;47:650e4. [36] Snyder JR, Olander HJ, Pascoe JR, Holland M, Kurpershoek CJ. Morphologic alterations observed during experimental ischemia of the equine large colon. Am J Vet Res 1988;49:801e9. [37] Ellis CM, Lynch TM, Slone DE, Hughes FE, Clark CK. Survival and complications after large colon resection and end-to-end anastomosis for strangulating large colon volvulus in seventy-three horses. Vet Surg 2008;37:786e90. [38] Suthers JM, Pinchbeck GL, Proudman CJ, Archer DC. Risk factors for large colon volvulus in the UK. Equine Vet J 2013;45:558e63. [39] Williams S, Horner J, Orton E, Green M, McMullen S, Mobasheri A, et al. Water intake, faecal output and intestinal motility in horses moved from pasture to a stabled management regime with controlled exercise. Equine Vet J 2015;47: 96e100. [40] White 2nd NA. Intestinal infarction associated with mesenteric vascular thrombotic disease in the horse. J Am Vet Med Assoc 1981;178: 259e62. [41] Pihl TH, Nielsen MK, Olsen SN, Leifsson PS, Jacobsen S. Nonstrangulating intestinal infarctions associated with Strongylus vulgaris: clinical presentation and treatment outcomes of 30 horses (2008-2016). Equine Vet J 2018;50: 474e80. [42] Weese JS, Holcombe SJ, Embertson RM, Kurtz KA, Roessner HA, Jalali M, et al. Changes in the faecal microbiota of mares precede the development of post partum colic. Equine Vet J 2015;47:641e9. [43] Schoster A, Arroyo LG, Staempfli HR, Weese JS. Comparison of microbial populations in the small intestine, large intestine and feces of healthy horses using terminal restriction fragment length polymorphism. BMC Res Notes 2013;6:91. [44] Daly K, Proudman CJ, Duncan SH, Flint HJ, Dyer J, Shirazi-Beechey SP. Alterations in microbiota and fermentation products in equine large intestine in response to dietary variation and intestinal disease. Br J Nutr 2012;107: 989e95.
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Journal of Equine Veterinary Science journal homepage: www.j-evs.com
Review Article
Colic Prevention to Avoid Colic Surgery: A Surgeon's Perspective Anthony T. Blikslager* Department of Clinical Sciences, North Carolina State University, Raleigh, North Carolina
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 February 2019 Received in revised form 26 February 2019 Accepted 26 February 2019 Available online 6 March 2019
Management factors associated with colic, particularly related to stall confinement and nutrition, have been linked to alterations in gastrointestinal mucosal transport, motility, and microbiome, which in turn creates conditions that induce colic. In particular, meal feeding creates large changes in water movement in and out of the colon and alters the microbiome. These conditions may in turn result in colic conditions such as large colon impaction or large colon volvulus. In addition, a range of management and nutritional factors have been found to place horses at risk of select colic conditions such as ileal impaction. Other specific colic conditions, such as strangulating lipomas, may be related to fat metabolism in geldings and ponies, although the association with nutrition and the endocrine system are less well defined. It has long been understood that parasites are associated with colic, and with the advent of highly effective anthelmintics, parasite-induced colic has been markedly reduced. Nonetheless, equine mangers and veterinarians have to be aware of changes in parasite resistance or patterns of activity, such as the resurgence of large strongyles with surveillance-based management of parasites. Overall, understanding management risk factors can lead to recommendations that prevent colic in horses. Additional study of these factors may ultimately lead to reductions in the prevalence of colic by suggesting optimal management practices. © 2019 Elsevier Inc. All rights reserved.
Keywords: Forage Impaction Volvulus Lipoma
1. Introduction Colic is in large part a disease syndrome associated with management. Horses evolved on the North American plains as hindgut fermenters, grazing forage for up to 18 hours/day while constantly moving. Management of horses by people has changed this activity to include stall confinement and meal feeding, both of which alter the physiology of the gastrointestinal tract by altering motility and the microbiome. These changes are associated with certain forms of colic, such as large colon impaction. In addition, nutrition may result in specific forms of colic, such as strangulating lipomas. Furthermore, vigilance related to management of parasites is critical because changes in parasite prevalence or resistance results in select forms of colic. Specific changes in gastrointestinal physiology induced by changes in management, as well as specific forms of
Animal welfare/ethical statement: No animals were used as a part of this review article. In addition, this article has not been submitted to another journal, and no abstract of this work has been submitted. Conflict of interest statement: I have no conflicts of interest to declare. No funding was used to generate this review. * Corresponding author at: Anthony T. Blikslager, College of Veterinary Medicine, 1060 William Moore Drive, Raleigh, NC 27607. E-mail address: [email protected]. https://doi.org/10.1016/j.jevs.2019.02.023 0737-0806/© 2019 Elsevier Inc. All rights reserved.
colic related to changes in nutrition, exercise, and deworming programs are discussed, including how colic may be prevented. 2. Prevalence of Colic in Horses According to a US national survey conducted in 2001, approximately 4% of horses have an episode of colic annually, with a case fatality rate of 11% [1]. Strangulating obstruction, a disease process in which simultaneous occlusion of the intestinal lumen and vasculature results in ischemic mucosal injury, is arguably the principal cause of colic-associated deaths in horses. For example, a study conducted in the United Kingdom in a general equine practice setting over 2 years showed that 14 of 200 (7%) horses evaluated for colic died, and 12 of these 14 deaths were associated with intestinal strangulation [2]. However, approximately 40% of horses with colic that require surgical intervention are associated with simple obstruction of the gastrointestinal tract [3], including impactions and ingestion of foreign bodies. It is this group of surgical patients that have the greatest chance of being prevented by optimal management practices. These practices generally include feeding a diet based principally on forage (with concentrate added if needed for performance and/or adequate body weight), as well as turnout and exercise for > 12 hours/24 hour per day. Before assessing specific types of impaction colic, it is first important to understand the physiology of the equine gastrointestinal tract.
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3. Physiologically Critical Features of the Equine Digestive Tract Horses use the digestive strategy of hindgut fermentation, during which ingested forage is rapidly passed from the stomach along the small intestine (in excess of 20m in the average 500 kg adult horse, with a transit time of approximately 120e180 minutes) and into the cecum and large colon [4]. This may be less efficient than the digestive strategy of foregut fermentation, noted in ruminants, where forage that has been partially digested in the forestomaches can then enter the small intestine for efficient absorption of nutrients [5]. However, selection pressure for speed in horses to run from predators (top speed, approximately 70 km/h) likely resulted in development of a hindgut, where a large gut chamber would not impede running. The equine hindgut is voluminous and folded to accommodate its length within the abdomen into a double horse-shoe configuration with a ventral colon (the lower horse-shoe) primarily functioning as the fermentation chamber, and the dorsal colon (the upper horse-shoe) taking on a predominant role in water absorption [6]. The pelvic flexure, which connects the ventral and dorsal colons, comprises a hairpin turn from the larger diameter ventral colon to the smaller diameter dorsal colon. Suboptimal management of horses, such as feeding of poor quality forage, may lead to ingesta obstructions (impactions), which are most commonly found at the pelvic flexure [7]. Impactions of indigestible luminal contents, most notably sand, tend to obstruct at a more distal flexure present between the right dorsal colon and the transverse colon [8]. The rapid passage of digesta along the small intestinal tract requires relatively large volumes of fluid, which are primarily secreted by the salivary glands, pancreas, and small intestinal mucosa [4]. The relative fluid volumes entering the equine digestive tract have been studied, and show that horses secrete approximately one extracellular fluid volume (calculated as 30% of body weight, or 150L in a 450 kg horse) into the digestive tract on a daily basis [4,6]. Control of absorption of NaCl and associated water movement across the equine colon has been studied in depth at both the local and systemic levels [6,9e12]. The endocrine-gut axis is critical to maintaining homeostasis considering the massive shift of fluid into and back out of the colon that occurs during the feeding of a meal, and this is accomplished by activating the reninangiotensin-aldosterone system interacting with colonic mucosal transporters [9,10,12]. This system is maximally activated during feeding of meals, which occurs during intensive management of horses [6]. In response to a single meal comprising the full ration for a horse in the form of hay-grain pellets, plasma renin activity was increased by 0.5 hours, followed by elevations in plasma aldosterone by 3 hours. The renin release was attributed to transient hypovolemia, as suggested by increases in plasma protein and packed cell volume [11]. This systemic hypovolemia is a consequence of fluid moving into the digestive tract. Studies have also shown that an increase in aldosterone in the horse results in a doubling of Naþ absorption in the proximal colon (ventral and dorsal colons), and a tripling of Naþ absorption in the distal colon as a mechanism to retrieve the large volumes of fluid that are secreted into the digestive tract [12]. Therefore, meal feeding places horses at risk of conditions such as colonic impaction, as a result of dramatic shifts in colonic fluid, or colonic distension, which can lead to colonic displacement or volvulus. 4. Simple Obstruction Simple intestinal obstruction is a physical obstruction of the lumen without obstruction of mesenteric vascular flow. The most common causes are intraluminal masses composed of feed material
(e.g., ileal impaction) or accumulation of parasites (e.g., ascarid impactions). There are other instances in which the bowel is obstructed without associated compromise of blood supply, for example, by extraluminal compression by a mass or band of tissue in horses with intraabdominal adhesions. The large volume of fluid entering the small intestinal lumen on a daily basis [10,12] causes the obstructed intestine to become distended. 4.1. Ascarid Impactions Impactions caused by Parascaris equorum typically occur in weanling foals that have been on a poor deworming program and that are administered an anthelmintic when they have a heavy parasite burden [13]. Products that cause sudden ascarid paralysis or death, including piperazine, organophosphates, and pyrantel pamoate, have been incriminated. However, it is likely that any effective broad-spectrum anthelmintic, such as the avermectins or moxidectin, will have the same effect. The lifecycle of Parascaris equorum includes ingestion of eggs from the pasture, migration into the lungs, and swallowing of larvae following coughing. Once in the intestine, the adult ascarids attain a length of up to 50 cm [13]. Therefore, it is critical to begin deworming foals at 4e6 weeks of age to prevent maturation of these parasites. In addition, there have been reported regional patterns of resistance to anthelmintics such as ivermectin [14], so that deworming programs require specific knowledge of which anthelmintics to use to reduce parasite burden while avoiding resistance. 4.2. Ileal Impaction Ileal impactions occur almost exclusively in adult horses in the southeastern United States. Although feeding of coastal Bermuda hay has been implicated in the regional distribution of this disease, it has been difficult to separate geographic location from regional hay sources as risk factors. However, a study from the southeastern United States showed that feeding coastal Bermuda hay and failing to deworm with an anthelmintic with efficacy against tapeworms are significant risk factors for ileal impaction [15]. Furthermore, in a study performed in the United Kingdom, horses with evidence of tapeworm (Anoplocephala perfoliata) infection were at risk for developing ileal impaction [16]. The latter likely results from an accumulation of mature tapeworms at the ileocecal junction. Tapeworms are difficult to surveil because the eggs rarely appear in a routine fecal flotation, although there is a serum test to test for antibodies to Anoplocephala perfoliate [16,17]. Routine deworming at least once annually for tapeworms is recommended. As far as the role of coastal Bermuda hay in ileal impactions, the precise reasons why it is associated with ileal impaction are unknown. However, it is a finer grass than other grasses, and there is the likelihood that when harvested for hay, an increased fiber level results in fine soft fibers that may be improperly chewed. The fibers then get caught in the ileocecal junction, ultimately blocking the passage of ingesta. The level of acid detergent fiber (ADF) or neutral detergent fiber (NDF) on a hay analysis that a horse can withstand is unknown because it likely also depends on individual horse factors such as dentition and familiarity with coastal Bermuda hay. Therefore, careful management practices include slow introduction of coastal Bermuda hay to horses that are not accustomed to this forage type, and use of the best quality coastal Bermuda hay because there is likely less room for error, as compared to other coarser grass hays. Hay quality can be related to digestibility, which is typically derived from in vivo trials. However, mathematical modeling has been used to derive dry matter digestibility (DMD) for horses from hay analyses, with the best models relating DMD to NDF and crude protein [18].
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4.3. Large Colon Impaction Impactions of the large colon with ingesta occur at sites of anatomic reductions in luminal diameter, particularly the pelvic flexure and the right dorsal colon [19]. Although there are a number of reported risk factors, most have not been proven. However, a sudden restriction in exercise associated with musculoskeletal injury appears to be frequently associated with onset of impaction. In addition, one study evaluating 120 horses with large colon impaction showed that 41% of cases were diagnosed in the winter [20], possibly related to reduced water intake or changes in diet. Equine feeding regimens may be very important in the development of large colon impactions. For example, twice-daily feeding of concentrate is associated with secretion of large volumes of fluid into the small intestine, resulting in transient hypovolemia (15% loss of plasma volume) [6]. This leads to activation of the reninangiotensin-aldosterone system, and because aldosterone stimulates absorption of fluid from the large colon, this may dehydrate colonic contents [6,12]. Large concentrate meals may decrease small intestinal transit time, resulting in increased presentation of soluble carbohydrate to the cecum and large colon. Large shifts of fluid into the colon occur as concentrates are readily fermented in the large intestine, which would be expected to activate the reninangiotensin-aldosterone system. This in turn triggers net fluid absorption from the large colon. The effects of these large fluid fluxes on development of large intestinal disorders remain to be fully characterized, but almost undoubtedly, they play some role in the syndrome of colic. From a practical standpoint, intestinal fluid fluxes may be reduced with frequent small feedings (dividing the ration into up to 6 equal portions) in those horses requiring concentrate to maintain condition [6,11]. In addition, presentation of soluble carbohydrate can trigger large shifts in the microbiome [21], which may lead to clinical syndromes such as endotoxemia and laminitis with rapid proliferation and breakdown of gramnegative bacteria [22]. 4.4. Sand Impactions of the Large Colon Sand impaction of the large colon is common in horses with access to sandy soils, particularly horses whose feed is placed on the ground. Sand accumulates in the large colon, primarily the right dorsal colon, but may be present in multiple locations [8,23]. In addition, sand may trigger diarrhea, presumably as a result of irritation of the colonic mucosa [24]. Sand is typically found in the feces, most simply by adding water to several fecal balls in a palpation sleeve and hanging the sleeve. If there is sand, it will collect in the fingers of the sleeve. Although the amount of sand in the feces does not necessarily correlate with accumulation of sand in the colon, it is advisable for owners to consider methods to reduce sand ingestion or increase sand clearance. Administration of psyllium hydrophilic mucilloid in water by stomach tube in an experimental study in which sand was surgically placed in the colon did not show increased clearance of sand with psyllium [25], but in horses with natural accumulations of sand, psyllium (1 g/kg body weight) in combination with magnesium sulfate (1 g/kg body weight) did significantly reduce the volume of sand (based on radiographs) [26]. However, there is no evidence of significant clearance of sand when feeding psyllium at home [27]. Nonetheless, more study of psyllium is likely warranted based on extensive anecdotal evidence for its ability to reduce the prevalence of sand colic. 5. Colic Associated with Ischemia Horses with strangulating lesions have consistently higher mortality rates, including preoperative and operative mortality in
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which horses with a poor prognosis based on the level of systemic inflammatory response syndrome may be electively euthanized before surgery, or horses at surgery may be euthanized because of the extent of injury or anatomical location [28,29]. Horses with intestinal diseases other than strangulating obstruction may also suffer from ischemic disease. For example, horses suffering from simple obstruction ultimately succumb to ischemic necrosis if not attended to medically and sometimes surgically as increasing intraluminal pressure progressively occludes the circulation within the intestinal wall [30,31]. Although strangulating obstruction is generally considered to be an “act of god” with no means of prevention, there are instances where management techniques may reduce the incidence of strangulating obstruction. In particular, there are two disease states of note that may be preventable: small intestinal strangulation by pedunculated lipoma and large colon volvulus. 5.1. Strangulation by Mesenteric Pedunculated Lipoma Lipomas form between the leaves of the mesentery as horses age, and mesenteric stalks likely develop as the weight of the lipoma tugs on the mesentery. The stalk of the lipoma and a loop of the small intestine or small colon may become intertwined, causing strangulation. Mature or aged horses (typically > 15 years of age) are at risk of strangulating lipomas [32]. In addition, geldings and ponies are also at risk for developing strangulating lipomas [32,33], which raises the possibility of alterations in metabolism and diet as possible risk factors. Although there have been no studies to assess the role of nutrition or gender on mesenteric fat deposition, there has been a study correlating body condition score with internal fat deposition [34]. There were significant correlations between body condition score and retroperitoneal fat, but not mesenteric fat, suggesting differences in fat deposition. However, further studies are warranted, particularly in populations of horses used for pleasure and sport activities that may be on a more lipogenic diet rather than the horses going to slaughter, which have been studied to date [34]. Ultimately, it may be possible to reduce the prevalence of lipomas with diet or by management of endocrinopathies in geldings and ponies. 5.2. Large Colon Volvulus This is the most fatal form of colic, although a recent study has shown that early recognition and surgical correction of the condition can result in a good outcome [35]. However, experimentally, the colon is irreversibly damaged with 3e4 hours of 360-degree volvulus of the entire colon [36], so that most horses not within a short distance of a referral hospital succumb to the disease. This should heighten interest in prevention of the disease. Large colon volvulus is most prevalent in peripartum Thoroughbred broodmares, although these is inherent bias in studies primarily from Thoroughbred breeding regions such as Lexington Kentucky [35] and Ocala Florida [37]. However, studies from the United Kingdom have revealed that broodmares that have a history of foaling are at risk regardless of breed [38]. Other interesting findings from this same study included management risk factors, such as an increase in the hours of stabling in the days leading up to colic, an increasing number of horses on the farm, and 3 or more people involved in the horse's care [38]. These factors all suggest that increased confinement or changes in foraging patterns are associated with colonic colic. Interestingly, increases in stabling has been studied in particular and shown to alter colonic motility [39]. Variables related to nutrition associated with increased risk of large colon volvulus included being fed hay in the last 28 days, being fed sugar-beet in the last 28 days, and an alteration in the amount of
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forage fed in the last 7 days. These may relate to the practicalities of managing broodmares in the peripartum period but also suggest that alterations in forage or digestible fiber may result in microbiome changes favoring a change in motility, a change in gasproducing bacteria, or both, thereby triggering initial gas distension and displacement of the colon. 5.3. Thromboembolic Colic In another form of ischemic disease, horses may suffer from nonstrangulating infarction, which is most commonly associated with parasite migration [40]. Although thromboemboli have been implicated in the pathogenesis of this disease, careful dissection of naturally occurring lesions has not revealed the presence of thrombi at the site of intestinal infarctions in most cases, suggesting that vasospasm plays an important role in this disease [40]. Although this disease process has become relatively rare with the advent of effective broad-spectrum anthelmintics, there has been a notable increase in infection with Strongylus vulgaris, the principal parasite that triggers thromboembolic colic [41]. This has partly resulted from surveillance-based deworming programs, primarily aimed at small strongyles. Therefore, careful assessment of deworming programs continues to be a critical component of management to reduce the incidence of colic. 6. The Equine Microbiome There has been recent interest in the equine microbiome and how it is altered under differing management practices. Numerous differences have been described in the fecal microbiota of postpartum mares that preceded colic (defined as an episode of abdominal pain based on the mare's behavior [pawing and rolling] that lasted >2 hours and required administration of analgesics). For example, one study found associations between changes in Firmicutes and Proteobacteria, most notably Lachnospiraceae and Ruminococcaceae, and the development of colic [42]. Furthermore, the authors of this study suggested that select changes in the fecal microbiota could possibly be used to predict higher risk of colic [42]. Although studies on equine microbiota have often focused on fecal microbiota, it has been shown that fecal microbiota are not reliably indicative of colonic microbiota [43]. Nonetheless, another study evaluating the effect of concentrate diet on colonic microbiota collected at the time of slaughter has shown some similar results to the aforementioned fecal microbiota study. In particular, feeding of dietary concentrate (the core diet for all concentrate-fed horses consisted of a coarse mix balancer (2e2.5 kg/d; 20e25 kJ digestible energy/g), hay/haylage (6 kg/d; 60 kJ digestible energy/ g), and barley (1 kg/d; 13 kJ digestible energy/g)) resulted in a significant increase in Lachnospiraceae [44]. This same study showed that horses fed concentrate diet (listed above) versus a grass-only diet had an increase in lactic acid-producing microbiota (the BacilluseLactobacilluseStreptococcus group) in their colonic contents (obtained following euthanasia), resulting in higher concentrations of lactic acid. Interestingly, the shift to lactic acidproducing microbiota was also associated with horses that developed colonic distension or impaction [44]. Despite changes that appear to be selective enough to be used to detect horses at risk of colic, a great deal of variability in individual horse microbiota even when managed under similar circumstances has been shown [43], suggesting caution when interpreting microbiome-related risk factors in individual or small groups of horses. Furthermore, with the number of different “concentrate” diets now available, including high-fat diets, and diets containing fiber, versus a pure grain concentrate diet, dietary factors would have to be assessed accurately as to which microbiome changes they may induce.
7. Conclusions When evaluating the evidence assessing the link between management and dietary factors and their association with colic, it is becoming increasingly clear that practices such as meal feeding and stalling of horses for the majority of the day (>12 hours) causes notable physiological changes, including changes in mucosal water transport [10], that can result in diseases as severe as large colon volvulus. Continued efforts to further evaluate the effects of equine management on the microbiome will likely provide more clues as to the pathogenesis of colic and a greater ability to institute preventive measures. These measures should continue to include simple techniques such as continuous access to forage and consistent daily exercise but continued provision of more specific advice related to deworming programs and the optimal diet to minimize daily fluctuations in colonic fluid flux and shifts in the microbiome should be provided to owners in an attempt to reduce the prevalence of colic. References [1] Traub-Dargatz JL, Kopral CA, Seitzinger AH, Garber LP, Forde K, White NA. Estimate of the national incidence of and operation-level risk factors for colic among horses in the United States, spring 1998 to spring 1999. J Am Vet Med Assoc 2001;219:67e71. [2] Proudman CJ. A two year, prospective survey of equine colic in general practice. Equine Vet J 1992;24:90e3. [3] Mair TS, Smith LJ. Survival and complication rates in 300 horses undergoing surgical treatment of colic. Part 1: short-term survival following a single laparotomy. Equine Vet J 2005;37:296e302. [4] Argenzio R. Physiology of digestive, secretory, and absorptive processes. In: White NA, editor. The equine acute abdomen. 1st ed. Philadelphia: Lea & Febiger; 1990. p. 25. [5] Janis C. The evolutionary strategy of the equidae and the origins of rumen and cecal digestion. Evolution 1976;30:757e74. [6] Clarke LL, Roberts MC, Argenzio RA. Feeding and digestive problems in horses. Physiologic responses to a concentrated meal. Vet Clin North Am Equine Pract 1990;6:433e50. [7] Dabareiner RM, White NA. Large colon impaction in horses: 147 cases (19851991). J Am Vet Med Assoc 1995;206:679e85. [8] Ragle CA, Meagher DM, Lacroix CA, Honnas CM. Surgical treatment of sand colic. Results in 40 horses. Vet Surg 1989;18:48e51. [9] Clarke LL, Argenzio RA. NaCl transport across equine proximal colon and the effect of endogenous prostanoids. Am J Physiol 1990;259:G62e9. [10] Clarke LL, Argenzio RA, Roberts MC. Effect of meal feeding on plasma volume and urinary electrolyte clearance in ponies. Am J Vet Res 1990;51:571e6. [11] Clarke LL, Ganjam VK, Fichtenbaum B, Hatfield D, Garner HE. Effect of feeding on renin-angiotensin-aldosterone system of the horse. Am J Physiol 1988;254:R524e30. [12] Clarke LL, Roberts MC, Grubb BR, Argenzio RA. Short-term effect of aldosterone on Na-Cl transport across equine colon. Am J Physiol 1992;262:R939e46. [13] Cribb NC, Cote NM, Boure LP, Peregrine AS. Acute small intestinal obstruction associated with Parascaris equorum infection in young horses: 25 cases (1985-2004). N Z Vet J 2006;54:338e43. [14] Lyons ET, Tolliver SC, Collins SS. Prevalence of large endoparasites at necropsy in horses infected with Population B small strongyles in a herd established in Kentucky in 1966. Parasitol Res 2006;99:114e8. [15] Little D, Blikslager AT. Factors associated with development of ileal impaction in horses with surgical colic: 78 cases (1986-2000). Equine Vet J 2002;34: 464e8. [16] Proudman CJ, French NP, Trees AJ. Tapeworm infection is a significant risk factor for spasmodic colic and ileal impaction colic in the horse. Equine Vet J 1998;30:194e9. [17] Barrett EJ, Farlam J, Proudman CJ. Field trial of the efficacy of a combination of ivermectin and praziquantel in horses infected with roundworms and tapeworms. Vet Rec 2004;154:323e5. [18] Hansen TL, Lawrence LM. Composition factors predicting forage digestibility by horses. J Equine Vet Sci 2017;58:97e102. [19] White 2nd NA, Dabareiner RM. Treatment of impaction colics. Vet Clin North Am Equine Pract 1997;13:243e59. [20] Jennings K, Curtis L, Burford J, Freeman S. Prospective survey of veterinary practitioners' primary assessment of equine colic: clinical features, diagnoses, and treatment of 120 cases of large colon impaction. BMC Vet Res 2014;10(suppl 1):S2. [21] Warzecha CM, Coverdale JA, Janecka JE, Leatherwood JL, Pinchak WE, Wickersham TA, et al. Influence of short-term dietary starch inclusion on the equine cecal microbiome. J Anim Sci 2017;95:5077e90.
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[34] Morrison PK, Harris PA, Maltin CA, Grove-White D, Argo CM. EQUIFAT: a novel scoring system for the semi-quantitative evaluation of regional adipose tissues in Equidae. PLoS One 2017;12:e0173753. [35] Hackett ES, Embertson RM, Hopper SA, Woodie JB, Ruggles AJ. Duration of disease influences survival to discharge of Thoroughbred mares with surgically treated large colon volvulus. Equine Vet J 2015;47:650e4. [36] Snyder JR, Olander HJ, Pascoe JR, Holland M, Kurpershoek CJ. Morphologic alterations observed during experimental ischemia of the equine large colon. Am J Vet Res 1988;49:801e9. [37] Ellis CM, Lynch TM, Slone DE, Hughes FE, Clark CK. Survival and complications after large colon resection and end-to-end anastomosis for strangulating large colon volvulus in seventy-three horses. Vet Surg 2008;37:786e90. [38] Suthers JM, Pinchbeck GL, Proudman CJ, Archer DC. Risk factors for large colon volvulus in the UK. Equine Vet J 2013;45:558e63. [39] Williams S, Horner J, Orton E, Green M, McMullen S, Mobasheri A, et al. Water intake, faecal output and intestinal motility in horses moved from pasture to a stabled management regime with controlled exercise. Equine Vet J 2015;47: 96e100. [40] White 2nd NA. Intestinal infarction associated with mesenteric vascular thrombotic disease in the horse. J Am Vet Med Assoc 1981;178: 259e62. [41] Pihl TH, Nielsen MK, Olsen SN, Leifsson PS, Jacobsen S. Nonstrangulating intestinal infarctions associated with Strongylus vulgaris: clinical presentation and treatment outcomes of 30 horses (2008-2016). Equine Vet J 2018;50: 474e80. [42] Weese JS, Holcombe SJ, Embertson RM, Kurtz KA, Roessner HA, Jalali M, et al. Changes in the faecal microbiota of mares precede the development of post partum colic. Equine Vet J 2015;47:641e9. [43] Schoster A, Arroyo LG, Staempfli HR, Weese JS. Comparison of microbial populations in the small intestine, large intestine and feces of healthy horses using terminal restriction fragment length polymorphism. BMC Res Notes 2013;6:91. [44] Daly K, Proudman CJ, Duncan SH, Flint HJ, Dyer J, Shirazi-Beechey SP. Alterations in microbiota and fermentation products in equine large intestine in response to dietary variation and intestinal disease. Br J Nutr 2012;107: 989e95.