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Endocrinopathic Laminitis, Obesity-Associated Laminitis, and Pasture-Associated Laminitis

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Endocrinopathic Laminitis, Obesity-Associated Laminitis, and Pasture-Associated Laminitis IN-DEPTH: LAMINITIS FOR THE PRACTITIONER Endocrinopathic Laminitis, Obesity-Associated Laminitis, and Pasture-Associated Laminitis Nicholas Frank, DVM, PhD, Diplomate ACVIM Author’s address: Department of Large Animal Clinical Sciences, University of Tennessee, 2407 River Drive, Knoxville, TN 37996; e-mail: [email protected]. © 2008 AAEP. 1. Introduction measuring blood insulin concentrations, which are In a recent online survey, we asked equine practi- usually elevated in affected horses. We hypothe- tioners to list the three most common causes of size that IR is the key determinant of laminitis sus- laminitis in horses seen within their practice. We ceptibility in horses, and this explains why specific expected veterinarians to list colitis, colic, and re- animals within a herd develop disease. This hypoth- tained placenta as the primary causes of laminitis, esis is supported by evidence that insulin-resistant but many respondents listed obesity, insulin resis- ponies are more likely to develop pasture-associated tance (IR), equine metabolic syndrome (EMS), pitu- laminitis and that laminitis can be experimentally itary pars intermedia dysfunction (PPID), and lush induced by infusing insulin intravenously.1,2 pasture. These results reflect the prevalence of en- Obesity-associated laminitis is a useful term be- docrine/metabolic problems in horses that are seen cause obesity is easily recognized, and owners can in general practice. We will examine these prob- address this issue to reduce the risk of laminitis. lems and discuss the potential mechanisms involved However, it has not been established whether obe- in endocrinopathic laminitis. sity per se raises the risk of laminitis or whether the disease is caused by IR, which is more common in 2. Terminology obese horses.3 Obesity and IR are associated in Insulin resistance is defined as the failure of tissues horses, but it is important to recognize that not to respond appropriately to insulin. There are nu- every obese horse is insulin resistant. Some ani- merous ways in which tissues become insulin resis- mals may be more tolerant of obesity, or it may take tant, including a reduction in the density of insulin a certain period of time for IR to develop. Obese receptors on the cell surface, malfunction of insulin horses might also be more susceptible to laminitis receptors, defective internal signaling pathways, because they are in a pro-inflammatory state. Obe- and interference with the translocation or function sity, inflammation, and IR are associated in humans of glucose transporter 4 (GLUT4) proteins. Obese because tumor necrosis factor ␣ (TNF␣) is secreted horses are more likely to suffer from IR, and insulin from adipose tissues as body mass index increases.4 sensitivity decreases when obesity is experimentally This inflammatory cytokine inhibits insulin receptor induced.a Insulin resistance can be diagnosed by signaling, which lowers insulin sensitivity. Vick et NOTES AAEP PROCEEDINGS ր Vol. 54 ր 2008 341 IN-DEPTH: LAMINITIS FOR THE PRACTITIONER al.5 found that blood TNF␣ mRNA expression was It is interesting to consider the idea of converging higher in obese horses, and our research group has endocrinopathies. Horses that are initially obese detected elevated TNF␣ mRNA expression within and insulin resistant then develop PPID as they get adipose tissues collected from obese insulin-resis- older. A transition is sometimes observed in mid- tant horses.b Insulin resistance may be the link dle age (10–20 yr) as obese horses begin to retain between obesity and laminitis in horses, but sys- their winter haircoat and start to lose skeletal mus- temic inflammation could also play a role in deter- cle mass. Horses may be at the highest risk for mining laminitis susceptibility. endocrinopathic laminitis at this time. Endocrinopathic laminitis is a general term that Pasture-associated laminitis is also called grass describes laminitis that develops in horses with en- founder and typically develops after the pasture docrine/metabolic disorders. This includes lamini- grass grows rapidly in the spring or after a heavy tis that is associated with obesity, IR, PPID (also rain. Pasture grazing contributes to obesity in called equine Cushing’s disease), or corticosteroid metabolically efficient horses because large amounts administration. of energy are consumed when grass is abundant. EMS is a term that has been adopted to describe a Sugars from pasture grass also exacerbate IR and clinical syndrome of obesity and/or regional adipos- contribute to the progression of this condition.1 ity, IR, and laminitis. This term is useful because It should also be recognized that lush pasture chal- it ties laminitis to IR. Grouping these problems lenges the gastrointestinal tract because grass is together as a clinical syndrome prompts the practi- consumed in large quantities over a relatively short tioner to test for IR and make recommendations to period of time. This increases the mass of feed control the problem. Horses of certain breeds and passing through the intestinal tract and therefore bloodlines are genetically predisposed to EMS. the total amount of carbohydrate entering the large In our practice, Morgan horses, Paso Finos, Arabi- intestine. The carbohydrate content and composi- ans, Tennessee Walking Horses, Warmbloods, and tion of the grass also varies markedly over time. pony breeds are at higher risk, but this syndrome Grass plants store carbohydrates when nutrients has been recognized in many other breeds. A more and sunlight are plentiful or when they are prepar- efficient energy metabolism seems to predispose an- ing for drought or winter conditions. Pasture graz- imals to obesity and consequently IR. Young to ing contributes to the development of obesity and IR middle-aged horses are affected, and there is an and represents a dynamic factor that may trigger important interaction with management practices. laminitis. Horses become obese and develop IR when they are fed too many calories in the form of grain or pasture 3. Relating IR to Laminitis grass. PPID is the most common endocrinopathy affect- Vasoconstriction ing horses. Older horses are affected, and hirsut- Insulin possesses vasoregulatory properties, and ism is a key feature of this disorder. Hirsutism this may explain why IR predisposes horses to lami- takes the form of a long curly haircoat in advanced nitis. Slow vasodilation occurs in response to insu- cases, but delayed shedding of the haircoat is an lin through the increased synthesis of nitric oxide early indicator of PPID. Skeletal muscle atrophy, (NO) from endothelial cells.8 However, insulin also polyuria, polydipsia, and laminitis are also clinical promotes vasoconstriction by stimulating the syn- signs of this condition.6 More research is needed to thesis of endothelin-1 (ET-1) and activating the sym- determine whether horses with PPID are predis- pathetic nervous system. posed to laminitis because corticosteroid excess Activation of the insulin receptor stimulates two weakens hoof tissues over time or whether IR is the different signaling pathways within the vascular en- key determinant of laminitis risk in these patients.7 dothelial cell. NO is secreted when the phosphati- Johnson et al.7 reviewed the potential effects of sys- dylinositol 3-kinase (PI3K) pathway is activated, temic or local cortisol excess on laminar tissues and whereas activation of the mitogen-activated protein blood vessels. kinase (MAPK) pathway leads to the release of Our experience suggests that horses with PPID ET-1. The effects of insulin on glucose uptake are that are also insulin resistant are more likely to mediated by PI3K, so this pathway is disrupted develop laminitis than those with normal insulin sen- when IR develops. Interestingly, this causes the sitivity. Pergolide is the treatment of choice for MAPK pathway to be stimulated and ET-1 synthesis PPID, and many horses respond positively to this increases. Vasoconstriction is promoted in the in- drug. This positive response often includes improve- sulin-resistant animal as NO production decreases, ment in insulin sensitivity because cortisol antago- and this may impair the ability of vessels to respond nizes the action of insulin and hyperadrenocorticism to vascular challenges. Eades et al.9 detected an abates in treated animals. Not all patients with increase in plasma ET-1 concentration within blood PPID suffer from IR. Insulin sensitivity seems to collected from digital veins 12 h after carbohydrate vary according to the body condition of the horse and was administered to induce laminitis in healthy stage of disease. Horses with PPID can have low, horses. This finding suggests that digital vessels normal, or enhanced insulin sensitivity. undergo vasoconstriction as a result of carbohydrate 342 2008 ր Vol. 54 ր AAEP PROCEEDINGS IN-DEPTH: LAMINITIS FOR THE PRACTITIONER overload in horses, which may contribute to the de- striction. It has been established that endotheli- velopment of laminitis. If that is the case, horses um-derived NO modulates the response to with chronic IR would be more likely to develop vasoconstrictors within the vasculature of the laminitis when challenged, because IR has already equine digit.18 promoted vasoconstriction. Capillary Recruitment Adhesion Molecules Chronic IR may have other effects on the vascula- These molecules are found on the surface of endo- ture because insulin is involved in capillary recruit- thelial cells and may play an important role in the ment.8 In humans, ingestion of a meal is development of laminitis. Loftus et al.10 detected associated with increased blood flow to limbs and higher mRNA expression of intracellular adhesion decreased vascular resistance.19 Terminal arte- molecule (ICAM) and E-selectin within laminar tis- rioles dilate, which increases the number of capillar- sues collected 1.5 h after black walnut extract was ies that are perfused. This is referred to as administered to induce laminitis. Insulin stimu- capillary recruitment, and it is a physiologic mech- lates the expression of vascular cell adhesion mole- anism that enhances glucose delivery to myocytes.8 cule (VCAM-1) and E-selectin through the MAPK In one study performed in humans, microvascular pathway.
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