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Compendium June 2013 (Vol 35, No 6)

Feline Small Cell Lymphosarcoma Versus Inflammatory Bowel Disease: Treatment and Prognosis

by Christian Eriksson de Rezende, DVM, MS, Suliman Al-Ghazlat, DVM, DACVIM

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    Abstract

    Feline inflammatory bowel disease is a diagnosis of exclusion and a common cause for chronic gastrointestinal signs such as weight loss, variation in appetite, vomiting, diarrhea, and lethargy. Patients with intestinal small cell lymphosarcoma can present with identical clinical signs, and differentiating between these two conditions can be a challenge. A companion article discusses the value of performing immunohistochemistry and polymerase chain reaction testing on intestinal biopsy samples for this purpose.

    Treatment for presumptive or diagnosed inflammatory bowel disease (IBD) includes dietary modification, antimicrobials with immunomodulatory properties, and glucocorticoids. For small cell lymphosarcoma (SCLSA), treatment with chlorambucil in conjunction with corticosteroids results in a favorable prognosis compared with other forms of lymphoma.

    The Role of Dietary Modification

    The use of a highly digestible diet with a novel source of protein is recommended for feline patients with suspected or confirmed IBD and may help by limiting the antigenic stimulation of the intestine’s mucosal immune system. The use of a hydrolyzed protein diet can also be effective, although these diets may be less palatable than those using a novel source of protein.1 In a 2001 study of cats with chronic gastrointestinal (GI) signs attributed to food allergies, IBD, or an unknown cause, approximately 50% of cats fed novel-protein diets showed resolution of clinical signs.2 Some studies also indicate that cats with food allergies or IBD may have significant improvement in clinical signs (e.g., vomiting, diarrhea) in as few as 4 to 8 days after dietary modification.2,3 Other sources argue that a period of 8 to 12 weeks may be needed before concluding that dietary modification is not helpful.4 It is essential that the pet receive only the trial food during this time (e.g., no treats, flavored drugs, or flavored chew toys should be given).4

    Novel-protein diets may help ameliorate clinical signs and potentially delay the need for immunosuppressive therapy for cats with IBD; however, the use of additional therapeutic interventions may be inevitable. For example, one study showed that although cats diagnosed with IBD had an improvement of clinical signs after being fed a novel protein diet, corticosteroids were necessary to sustain remission.5 In other research, a dietary trial alone was unsuccessful in controlling clinical signs in cats.6 Based on the current state of understanding regarding the pathophysiology of IBD, the use of a novel protein diet is still recommended early in the treatment process, knowing that it may not suffice to control clinical signs. If the patient is inappetent, an appetite stimulant (e.g., mirtazapine 2 to 3 mg/cat PO q72h or cyproheptadine 1 to 2 mg/cat PO q12h) may be necessary.7 Sometimes, immunosuppressive therapy in combination with glucocorticoids may need to be started before a dietary change can be accomplished.

    Fiber-enriched diets have been reported to be useful in patients with colonic IBD, but there is no evidence that they are particularly helpful in patients with IBD affecting the small intestine.8

    The role of diet in the management of SCLSA should follow the same principles that apply to cats with disease of the GI tract. Dietary factors that should be considered include (1) using highly digestible nutrients (protein digestibility of >87%; fat/carbohydrate digestibility of >90%) and single protein and carbohydrate ingredients if possible and (2) avoiding additives or flavoring that could promote dietary intolerance.4 Diets containing a high-quality protein source are more easily digested and may result in improved assimilation of nutrients.4

    Key Points

    • While novel diets may ameliorate clinical signs of IBD, the use of corticosteroids may be necessary to sustain disease remission.
    • In cases of refractory IBD, the clinician should consider lack of client compliance with treatment, other comorbidities, or a misdiagnosis (SCLSA instead of IBD) before altering therapy.
    • Clients should be educated about the potential for a favorable prognosis for cats with SCLSA.

    The use of omega-3 fatty acids has been described as adjunctive therapy in patients with inflammatory diseases because they may help decrease the concentrations of proinflammatory omega-6 metabolites (e.g., prostaglandins, interleukin-1).9 Although studies have evaluated the use of fatty acids in the management of various feline disorders (e.g., atopic dermatitis, renal disease, osteoarthritis), we are not aware of trials assessing efficacy in the management of IBD. Because most commercial feline diets are augmented with omega-3 fatty acids, additional supplementation may not be necessary. Furthermore, omega-3 fatty acids can be unpalatable and cause diarrhea, and their long-term safety has not been determined in cats.1,9

    Probiotics, Prebiotics and Synbiotics

    Probiotics have been defined as live microorganisms that confer a health benefit to the host when administered in adequate amounts.10 The proposed mechanisms for the benefits of probiotics in human IBD include their ability to prevent gut colonization by pathogenic bacteria, reduce inflammatory cytokine expression, enhance epithelial cell proliferation, inhibit apoptosis, and provide metabolic energy for enterocytes.11

    Probiotics are being investigated as an adjunctive therapeutic option in various conditions in people, such as allergies in children and recurring urinary tract infections.10 The use of probiotics has been shown to be efficacious in ameliorating symptoms and maintaining remission in such conditions as ulcerative colitis, pouchitis, and antibiotic-associated diarrhea in humans.11

    The efficacy of using probiotics for the specific management of feline IBD or SCLSA has not been established; however, reports have shown that probiotics can improve the intestinal environment and the function of the immune system. One study showed that the probiotic strain Lactobacillus acidophilus DSM 13241 favorably altered the intestinal microflora in healthy adult cats by increasing and decreasing the populations of beneficial (e.g., Lactobacillus spp) and detrimental (Clostridium and Enterococcus spp) bacteria, respectively.12 Beneficial immunomodulatory effects were also noted, such as altered lymphocyte and eosinophil populations and an increase in phagocytic activity of granulocytes. Cats receiving probiotics also had a lowered concentration of endotoxins.12 Another study identified higher percentages of CD4+ lymphocytes in vaccinated pathogen-free kittens treated with Enterococcus faecium SF68 when compared with controls.13 These studies support the potential for probiotics to favorably alter the GI microbiota and immune function of cats.

    Once started, it is likely that probiotic therapy may need to be continued indefinitely. If stopped, the number of probiotic organisms may gradually decrease in the feces, possibly voiding some of the therapy’s beneficial effects.12,13

    The use of probiotics appears to be safe in animals but may need to be used with caution in severely immunosuppressed or critically ill animals, as human cases of bacteremia from probiotic strains such as Bacillus subtilis and Lactobacillus spp have been reported.10

    Choosing which probiotic to use can be challenging, as studies have shown that commercial products have a large variation in quality control.12 Products may not possess viable organisms or the recommended dose of at least 109 organisms.12 Additionally, products may frequently contain improper labels (e.g., misidentification of bacteria).14 For these reasons, practitioners should carefully evaluate the label, looking for the names and numbers of all organisms included and their expected viability, both when administered (shelf-life) as well as at the level of the intestine (protection from digestion).14 Due to a limited number of objective studies evaluating the efficacy of prebiotics and probiotics, we prefer products from reputable companies or those that have been independently clinically evaluated.

    Prebiotics are described as “non-digestible food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one, or a limited number of bacteria in the colon, thus providing host health.”11 Common prebiotics used in veterinary medicine include chicory (inulin) and beet pulp (incorporated into some commercial diets) and oligosaccharides such as fructo-oligosaccharide. The fermentation of these ingredients may help increase populations of beneficial gut bacteria (e.g., Lactobacillus and Bifidobacterium spp) that produce butyrate, a short-chain fatty acid that promotes colonic health. At this time, we are not aware of data that convincingly justify the use of prebiotics exclusively as an effective adjunct therapy for the treatment of IBD or SCLSA in cats. A recent meta-analysis evaluated the effects of various prebiotics on digestibility, short-chain fatty acid concentration, and gut bacterial populations in dogs fed various prebiotics (e.g., inulin, fructo-oligosaccharides). This study concluded that the use of prebiotics may increase the number of beneficial bacteria and levels of short-chain fatty acids that are beneficial for gut health.15

    Products called synbiotics contain both prebiotic sugars and probiotic bacteria. In a recent report, cats with chronic diarrhea had an improvement in their fecal scores after being fed a proprietary synbiotic for 21 days.16

    Cobalamin

    Cobalamin (vitamin B12) is a required cofactor for normal nucleic acid synthesis and hematopoiesis. Vitamin B12 is absorbed by specific receptors located in the ileum; therefore, pathology in this area of the intestine can result in hypocobalaminemia. Although cobalamin supplementation does not treat the underlying GI disease (e.g., IBD or SCLSA), it appears to improve the clinical state of most affected cats; it may be required for optimal response to immunosuppressive therapy.17 It should be administered subcutaneously at a dosage of 250 mg once a week for 6 weeks, then every other week for 6 weeks, then monthly if serum cobalamin levels are <300 ng/L.18,19 We recommend that practitioners consider rechecking cobalamin levels after four injections to ensure that adequate serum levels have been achieved, and then periodically during the patient’s treatment. Recurrence of clinical signs (e.g., weight loss, vomiting, diarrhea) warrants reevaluation of cobalamin levels.

    Immunosuppressive Therapy

    Corticosteroids are the cornerstone of therapy for IBD and SCLSA and have multiple effects on the immune system. They decrease leukocyte chemotaxis and cause lymphocytes and monocytes to redistribute to the lymphatic system. They exert antiinflammatory effects by inducing lipocortin-1, an inhibitor of phospholipase A2, thereby resulting in a decrease in inflammatory eicosanoids from arachidonic acid.20

    Prednisolone

    Prednisolone has a higher bioavailability than prednisone in cats and is therefore the preferred form.20 Although several tapering regimens are available for the treatment of IBD, a starting dose of 2 to 4 mg/kg/d (SID or divided BID) is used for 2 to 4 weeks. Once a favorable response is noted, the dose can be continued for an additional 2 to 4 weeks to ensure that the response was not fortuitous.8 At this time, a slow taper (e.g., dose reduction by 25% to 50% every 2 to 4 weeks) can be started with the goal of achieving the lowest effective dose that keeps the patient free of clinical signs. In some cases, prednisolone can be discontinued and the patient maintained on a novel protein diet and possibly an additional immunomodulatory agent (e.g., metronidazole). If a liquid corticosteroid formulation is used, ensure that it does not contain flavoring because additives of animal origin could interfere with disease remission.

    The use of methylprednisolone acetate at 10 mg/kg SC every 2 to 4 weeks has been advocated for patients that do not tolerate oral medication. The frequency of injections can be decreased to every 4 to 8 weeks depending on response to therapy. Long-acting corticosteroids are not generally recommended because the drawbacks include unpredictable bioavailability, predisposition to the patient becoming refractory to the agent, and the development of diabetes mellitus.

    Budesonide

    Budesonide is an orally administered glucocorticoid that was developed for humans with enteritis affecting the ileum and proximal colon (e.g., Crohn disease). Budesonide undergoes extensive first-pass hepatic metabolism in humans (>90% of available drug is converted to less active metabolites) and therefore causes minimal systemic effects. The efficacy of this medication is somewhat less than that of conventional corticosteroids in humans.21

    Studies evaluating the efficacy of budesonide in the treatment of IBD in companion animals are limited; however, there is some anecdotal evidence of success.22 A study of budesonide in dogs with IBD showed that a dose of 3 mg/m2 did significantly suppress the pituitary-adrenal axis, which did not correlate with clinical signs of excess glucocorticoids.23 To our knowledge, there are no studies evaluating the efficacy of budesonide in cats with IBD; however, empirical dosages of 0.5 to 1.0 mg/cat/d have been suggested.1,24

    Chlorambucil

    Chlorambucil is a nitrogen mustard derivative that acts as an alkylating agent. It cross-links deoxyribonucleic acid (DNA) and ribonucleic acid (RNA), which ultimately interferes with protein synthesis.25 Some sources recommend reserving this medication for patients with severe or relapsing IBD.8 This medication is used in conjunction with steroids at a dose of 2 mg PO every other day or every third day in cats weighing >4 kg or <4 kg, respectively.19 It is important to monitor the patient’s complete blood count (CBC) every 2 to 4 weeks when using this protocol because this agent can cause bone marrow suppression and permanent damage.26 Particular attention must be paid to declining neutrophil or platelet counts.

    Cyclosporine

    Cyclosporine inhibits T-cell activation and survival by inhibiting the production of cytokines, such as interleukin-2, that are necessary for T-cell viability.27 It has been used in dogs with IBD that is refractory to steroid therapy.27 Cyclosporine is used for several dermatologic conditions in dogs and cats (e.g., eosinophilic granuloma complex, pemphigus complex) and, recently, as adjunctive therapy for cats with idiopathic pure red cell aplasia.28 Anecdotally, cyclosporine has been used to treat IBD in cats with some success at a dose of 5 mg/kg PO once to twice daily.1 A recent study looking at adverse effects of cyclosporine in cats treated for allergic skin disease (mean and median doses of cyclosporine were 5.25 mg/kg and 5 mg/kg, respectively) reported vomiting, diarrhea, anorexia, and weight loss as the most common adverse events.29 These effects may lead the clinician to reduce the dose or frequency or be severe enough to require discontinuation of the drug (discontinuation was reported in up to 10% of cats in the study). Other potential complications include hepatopathy, urinary tract infection, gingival hypertrophy, and, at very high doses, recrudescence of dormant toxoplasmosis.29

    Azathioprine

    Azathioprine is a synthetic purine analog that interferes with DNA replication and transcription in cells of the humoral and cell-mediated branches of the immune system.24 This drug is generally not recommended for use in cats due to reported severe bone marrow suppression and idiosyncratic fatal leukopenia and thrombocytopenia.24 A dose has been published for treatment of severe or refractory IBD (TABLE 1), with improvement seen in 3 to 5 weeks.8

    Antimicrobials

    Antibiotics can be used to treat conditions in which alteration of intestinal microbiota is desired (e.g., hepatic encephalopathy, IBD). Metronidazole is effective against anaerobic bacteria and protozoa and appears to affect cell-mediated immunity.8 The immunomodulatory effect of metronidazole is not clearly understood, but research has shown that it can induce DNA single-strand breaks in lymphocytes, suppress macrophage phagocytic activity by inhibiting macrophage tumor necrosis factor aproduction, and inhibit leukocyte-endothelial cell adhesion in venules.30 It may be effective as a sole agent in patients that have mild intestinal inflammation or used in conjunction with a glucocorticoid. In the latter case, the steroid should be tapered to every other day before the dose of metronidazole is reduced and eventually discontinued.8 Neurotoxicity (disorientation, ataxia, seizures, blindness) is the main adverse effect and usually resolves when the drug is discontinued.

    Tylosin is a bacteriostatic macrolide that is efficacious against gram-positive and gram-negative cocci and Mycoplasma spp. Escherichia coli and Salmonella spp are usually resistant to this macrolide. This antibiotic may alter the microflora favorably and may have antiinflammatory properties. It has been used more commonly to treat colonic IBD in dogs and cats.19

    Specific Treatment for Small Cell Lymphosarcoma

    Due to the indolent nature of SCLSA, treatment generally involvesa glucocorticoid (prednisolone) used in conjunction with chlorambucil, which targets slowly dividing lymphocytes.31 A standardized protocol does not exist, particularly with respect to the use of chlorambucil. The prednisolone regimen is typically started at an immunosuppressive dose (e.g., 2 to 3 mg/kg PO q24h or a standard dose of 5 to 10 mg/cat/d), and then reduced to 1 to 2 mg/kg/d once solid remission is achieved (resolution of clinical signs such as vomiting, diarrhea, and weight loss). Some clinicians maintain this daily dose for an extended time (e.g., 6 to 12 months) whereas others taper the corticosteroid regimen to every other day when remission is achieved.

    Chlorambucil is used in a continuous dosing regimen (e.g., 2 mg/cat PO q48–72h) or as a bolus (20 mg/m2 PO) every 2 to 3 weeks.32 The duration of clinical remission achieved with both regimens is comparable. Further studies are necessary to establish the optimal glucocorticoid/chlorambucil protocol, but administering chlorambucil every 2 to 3 weeks instead of every 2 to 3 days is a clear advantage. Stein et al32 reported treatment delays due to adverse hematologic effects in three of 28 cats receiving chlorambucil as a bolus therapy (two cases of neutropenia and one case of thrombocytopenia). These adverse effects resolved and did not require additional therapy.32

    Permanent bone marrow damage can occur when alkylating agents are used long term; therefore, it is important to monitor cats on chlorambucil for dropping trends in neutrophil and platelet counts.26 The CBC should be monitored during therapy. When using chlorambucil on a bi- or triweekly basis, a CBC is performed weekly for the first few doses of chemotherapy.26 Once it has been established that the dose is safe for the patient, a CBC can be evaluated before each dose (every 2 to 3 weeks) and then before every other dose (every 4 to 6 weeks).26 The drug should be discontinued if the patient’s segmented neutrophil and platelet counts are at or persistently below 1500 and/or 75,000 cells/mL, respectively.26 Rescue protocols using cyclophosphamide or combined therapy (cyclophosphamide, vincristine, prednisolone) have been used for patients that no longer respond to glucocorticoid-chlorambucil therapy.32

    Prognosis

    Incorporating immunohistochemistry (IHC) early in the diagnostic approach in conjunction with clonality evaluation in selected cases can significantly improve the ability to differentiate IBD from SCLSA and consequently establish a more accurate prognosis. All cases with a morphologic diagnosis of lymphoma or suspected lymphoma should be further evaluated by IHC. The presence of a monomorphic population of B or T lymphocytes supports the diagnosis of lymphoma.In cases in which a definitive diagnosis cannot be made, the clinician should request polymerase chain reaction testing for B and/or T cell clonality. If a clonal population is not present, then inflammation should be considered the most likely underlying disease process. Furthermore, if biopsies yield a morphologic diagnosis of IBD but the patient does not respond to conventional therapy, the clinician should consider repeating the biopsy or having the original samples reviewed in conjunction with IHC and PCR. The clinician must consider the quality and type of biopsy when interpreting results (e.g., full-thickness biopsies may reveal lymphocytic infiltration beyond the mucosa, which could be missed with endoscopic biopsy samples. In his recent study, Dr. Kiupel stresses that it is important to maintain a systematic approach to biopsy samples (histopathology followed by IHC and PCR) to increase the chances of achieving a correct diagnosis and selecting the best treatment.33

    Feline IBD can be well managed with a combination of dietary modification and immunosuppression; however, the client must be informed that cure is unlikely and the objective of treatment is to minimize frequency and intensity of clinical signs. In one study, 79% of cats treated with a change in diet and prednisone responded favorably to therapy.6 A more guarded prognosis may need to be discussed with clients if the patient is severely debilitated and or has severe histologic GI lesions, eosinophilic enteritis, or hypereosinophilic syndrome.

    In cases of refractory IBD, the clinician must determine if the client is being compliant with therapy (e.g., has the client altered the diet or decreased/discontinued drug therapy; is the client having difficulties medicating the animal). It is also possible that the patient has a more severe form of IBD (e.g., eosinophilic enteritis, hypereosinophilic syndrome). Alternatively, the patient may have comorbidities that were missed or have developed since the start of treatment (e.g., pancreatitis, cholangitis). Ultimately, the clinician must question whether the diagnosis of IBD is correct and whether the patient has SCLSA.34 In such cases, the clinician should consider collecting GI biopsy samples for histologic assessment followed by immunophenotyping and PCR for T-cell clonality if necessary, as discussed above.33

    The prognosis for cats with SCLSA affecting the GI system or other organs is also favorable, with one study by Kiselow et al reporting a 92% response rate for a median of >2.5 years (TABLE 2).35 This study indicated that the median response duration time was longer (29 months) for cats that had a complete response to treatment compared with partial responders (14 months). Although this study did not find an association between response to treatment and overall survival, other studies showed longer survival times for cats that achieved complete remission.35–37 Kiselow et al identified a large percentage of cats that were hypocobalaminemic (78%), which was associated with a shorter duration of remission but not overall survival time. Patients that experience relapse may be rescued with therapy consisting of cyclophosphamide and glucocorticoids, resulting in a 100% response rate in one study.32

    Downloadable PDF

    References

    1. Trepanier L. Idiopathic inflammatory bowel disease in cats—rational treatment selection. J Feline Med Surg 2009;11:32-38.

    2. Guilford WG, Jones BR, Markwell PJ, et al. Food sensitivity in cats with chronic idiopathic gastrointestinal problems. J Vet Intern Med 2001;15:7-13.

    3. Mandigers PJ, Biourge V, German AJ. Efficacy of a commercial hydrolysate diet in eight cats suffering from inflammatory bowel disease or adverse reaction to food. Tijdschr Diergeneeskd 2010;135:668-672.

    4. Zoran DL. Nutritional management of feline gastrointestinal diseases. Top Companion Anim Med 2008;23:200-206.

    5. Dennis JS, Kruger JM, Mullaney TP. Lymphocytic-plasmacytic gastroenteritis in cats: 14 cases (1985-1990). J Am Vet Med Assoc 1992;200:1712-1718.

    6. Hart JR, Shaker E, Patnaik AK. Lymphocytic-plasmacytic enterocolitis in cats: 60 cases (1988–1990). J Am Anim Hosp Assoc 1994;30:505-514.

    7. Caney S. Weight loss in the elderly cat. Appetite is fine and everything looks normal... J Feline Med Surg 2009;11:738-746.

    8. Willard MD. Feline inflammatory bowel disease: a review. J Feline Med Surg 1999;1:155-164.

    9. Bauer JE. Therapeutic use of fish oils in companion animals. J Am Vet Med Assoc 2011;239:1441-1451.

    10. Wynn SG. Probiotics in veterinary practice. J Am Vet Med Assoc 2009;234:606-613.

    11. Geier MS, Bulter RN, Howarth GS. Inflammatory bowel disease: current insights into pathogenesis and new therapeutic options; probiotics, prebiotics and synbiotics. Int J Food Microbiol 2007;115:1-11.

    12. Marshall-Jones ZV, Baillon MLA, Croft JM, et al. Effects of Lactobacillus acidophilus DSM13241 as a probiotic in healthy adult cats. Am J Vet Res 2006;67:1005-1012.

    13. Vier JK, Knorr R, Cavadini C, et al. Effect of supplementation with Enterococcus faecium (SF68) on immune functions in cats. Vet Ther 2007;8:229-238.

    14. Weese JS. Evaluation of deficiencies in labeling of commercial probiotics. Can Vet J 2003;44:982-983.

    15. Patra AK. Responses of feeding prebiotics on nutrient digestibility, faecal microbiota composition and short-chain fatty acid concentrations in dogs: a meta-analysis. Animal 2011;5:1743-1750.

    16. Hart ML, Suchodolski JS, Steiner JM et al. Open-label trial of a multi-strain symbiotic in cats with chronic diarrhea. J Feline Med Surg 2012;14:240-245.

    17. Ruaux CG, Steiner JM, Williams DA. Early biochemical and clinical responses to cobalamin supplementation in cats with signs of gastrointestinal disease and severe hypocobalaminemia. J Vet Intern Med 2005;19:155-160.

    18. Ruaux CG, Steiner JM, Williams DA. Relationships between low serum cobalamin concentrations and methlymalonic academia in cats. J Vet Intern Med 2009;23:472-475.

    19. Ferguson D, Gaschen F. Feline idiopathic inflammatory bowel disease. Vet Focus 2009;19(2):20-30.

    20. Lowe AD, Campbell KL, Graves T. Glucocorticoids in the cat. Vet Dermatol 2008;19:340-347.

    21. Podolsky DK: Inflammatory bowel disease. N Engl J Med 2002;347:417-429.

    22. Stroup ST, Behrend EN, Kemppainen RJ, et al. Effects of oral administration of controlled-ileal-release budesonide and assessment of pituitary-adrenocortical axis suppression in clinically normal dogs. Am J Vet Res 2006;67:1173-1178.

    23. Tumulty JW, Broussard JD, Steiner JM, et al. Clinical effects of short-term oral budesonide on the hypothalamic-pituitary-adrenal axis in dogs with inflammatory bowel disease. J Am Anim Hosp Assoc 2004;40:120-123.

    24. Krecic MR. Feline inflammatory bowel disease: treatment, prognosis, and new developments. Compend Contin Educ Vet 2001;23:964-973.

    25. Benitah N, de Lorimier LP, Gaspar M, et al. Chlorambucil-induced myoclonus in a cat with lymphoma. J Am Anim Hosp Assoc 2003;39:283-287.

    26. Wilson HM. Feline alimentary lymphoma: demystifying the enigma. Top Companion Anim Med 2008;23:177-184.

    27. Allenspach K, Rüfenacht S, Sauter S, et al. Pharmacokinetics and clinical efficacy of cyclosporine treatment of dogs with steroid-refractory inflammatory bowel disease. J Vet Intern Med 2006;20:239-244.

    28. Viviano KR, Webb JL. Clinical use of cyclosporine as an adjunctive therapy in the management of feline idiopathic pure red cell aplasia. J Feline Med Surg 2011;13:885-895.

    29. Heinrich NA, McKeever PJ, Eisenschenk MC. Adverse events in 50 cats with allergic dermatitis receiving ciclosporin. Vet Dermatol 2011;22:511-520.

    30. Fararjeh M, Mohammad MK, Bustanji Y, et al. Evaluation of immunosuppression induced by metronidazole in Balb/c mice and human peripheral blood lymphocytes. Int Immunopharm 2008;8:341-350.

    31. Gieger T. Alimentary lymphoma in cats and dogs. Vet Clin North Am Small Anim Pract 2011;41:419-432.

    32. Stein TJ, Pellin M, Steinberg H, Chun R. Treatment of feline gastrointestinal small-cell lymphoma with chlorambucil and glucocorticoids. J Am Anim Hosp Assoc 2010;46:413-417.

    33. Kiupel M, Smedley RC, Pfent C, et al. Diagnostic algorithm to differentiate lymphoma from inflammation in feline small intestinal biopsy samples. Vet Pathol 2011;48:212-222.

    34. Jergens AE. Managing the refractory case of feline IBD. J Feline Med Surg 2003;5:47-50.

    35. Kiselow MA, Rassnick KM, McDonough SP, et al. Outcome of cats with low-grade lymphocytic lymphoma: 41 cases (1995–2005). J Am Vet Med Assoc 2008;232(3):405-410.

    36. Fondacaro JV, Richter KP, Carpenter JL. Feline gastrointestinal lymphoma: 67 cases (1988–1996). Eur J Comp Gastroenterol 1999;4:5-11.

    37. Lingard AE, Briscoe K, Beatty JA, et al. Low-grade alimentary lymphoma: clinicopathological findings and response to treatment in 17 cases. J Feline Med Surg 2009;11:692-700.

    References »

    NEXT: Focus on Nutrition: Dietary Management of Gastrointestinal Disease

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