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Ovariohysterectomy alters body composition and adipose and skeletal muscle gene expression in cats fed a high-protein or moderate-protein diet

Published online by Cambridge University Press:  28 May 2009

B. M. Vester
Affiliation:
Department of Animal Sciences, University of Illinois, Urbana, IL 61801, USA
S. M. Sutter
Affiliation:
Department of Animal Sciences, University of Illinois, Urbana, IL 61801, USA
T. L. Keel
Affiliation:
Department of Veterinary Clinical Medicine, University of Illinois, Urbana, IL 61801, USA
T. K. Graves
Affiliation:
Department of Veterinary Clinical Medicine, University of Illinois, Urbana, IL 61801, USA
K. S. Swanson*
Affiliation:
Department of Animal Sciences, University of Illinois, Urbana, IL 61801, USA
*
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Abstract

The objective of this study was to measure changes in body composition, physical activity and adipose and skeletal muscle gene expression of cats fed a high-protein (HP) diet or moderate-protein (MP) diet, following ovariohysterectomy. Eight cats were randomized onto HP or MP diets and were fed those diets for several months prior to baseline. All cats underwent an ovariohysterectomy at baseline (week 0) and were allowed ad libitum access to dietary treatments for 24 weeks. Food intake was measured daily, and BW and body condition score were measured weekly. Blood, adipose and skeletal muscle tissue samples were collected, physical activity was measured, and body composition was determined using DEXA (dual-energy X-ray absorptiometry) at weeks 0, 12 and 24. Caloric intake increased soon after ovariohysterectomy, resulting in increased (P < 0.05) BW at weeks 12 and 24 compared to week 0. Body condition score and body fat percentage increased (P < 0.05) over time. Blood glucose increased (P < 0.05) linearly over time. Non-esterified fatty acids were decreased (P < 0.05) at weeks 12 and 24 compared to week 0. Blood leptin increased (P < 0.05) over time. Total physical activity decreased (P < 0.05) from week 0 to weeks 12 and 24 in all cats. Adipose tissue mRNA abundance of adiponectin, hormone sensitive lipase, toll-like receptor-4, uncoupling protein-2 (UCP2) and vascular endothelial growth factor decreased (P < 0.05) linearly over time, regardless of diet. Skeletal muscle mRNA abundance for glucose transporter-1, hormone sensitive lipase and UCP2 were decreased (P < 0.05), regardless of dietary treatment. Our research noted metabolic changes following ovariohysterectomy that are in agreement with gene expression changes pertaining to lipid metabolism. Feeding cats ad libitum after ovariohysterectomy is inadvisable.

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Full Paper
Copyright
Copyright © The Animal Consortium 2009

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References

Ainslie, DA, Morris, MJ, Wittert, G, Turnbull, H, Proietto, J, Thornburn, AW 2001. Estrogen deficiency causes central leptin insensitivity and increased hypothalamic neuropeptide Y. International Journal of Obesity 25, 16801688.CrossRefGoogle ScholarPubMed
Allan, FJ, Pfeiffer, DU, Jones, BR, Esslemont, DH, Wiseman, MS 2000. A cross-sectional study of risk factors for obesity in cats in New Zealand. Preventive Veterinary Medicine 46, 183196.CrossRefGoogle ScholarPubMed
American Association of Cereal Chemists 1983. Approved methods, 8th edition. AACC, St. Paul, MN, USA.Google Scholar
Appleton, DJ, Rand, JS, Sunvold, GD 2000. Plasma leptin concentrations in cats: reference range, effect of weight gain and relationship with adiposity as measured by dual energy X-ray absorptiometry. Journal of Feline Medicine and Surgery 2, 191199.CrossRefGoogle ScholarPubMed
Association of Official Analytical Chemists 1984. Official methods of analysis, 14th edition. AOAC, Washington, DC, USA.Google Scholar
Association of Official Analytical Chemists 1995. Official methods of analysis, 15th edition. AOAC, Washington, DC, USA.Google Scholar
Backus, RC, Cave, NJ, Keisler, DH 2007. Gonadectomy and high dietary fat but not high dietary carbohydrate induce gains in body weight and fat of domestic cats. British Journal of Nutrition 98, 641650.CrossRefGoogle Scholar
Backus, RC, Havel, PJ, Gingerich, RL, Rogers, QR 2000. Relationship between serum leptin immunoreactivity and body fat mass as estimated by use of a novel gas-phase fourier transform infrared spectroscopy deuterium dilution method in cats. American Journal of Veterinary Research 61, 796801.CrossRefGoogle ScholarPubMed
Backus, RC, Rosenquist, GL, Rogers, QR, Calam, J, Morris, JG 1995. Elevation of plasma cholecystokinin (CCK) immunoreactivity by fat, protein, and amino acids in the cat, a carnivore. Regulatory Peptides 57, 123131.CrossRefGoogle Scholar
Bastard, J, Maachi, M, Tran Van Nhieu, J, Jardel, C, Bruckert, E, Grimaldi, A, Robert, J, Capeau, J, Hainque, B 2002. Adipose tissue IL-6 content correlates with resistance to insulin activation of glucose uptake in both in vivo and in vitro. Journal of Clinical Endocrinology and Metabolism 87, 20842089.CrossRefGoogle ScholarPubMed
Belsito, KR, Vester, BM, Keel, T, Graves, TK, Swanson, KS 2009. Impact of ovariohysterectomy and food intake on body composition, physical activity, and adipose gene expression in cats. Journal of Animal Science 87, 594602.CrossRefGoogle ScholarPubMed
Blaak, EE, Van Baak, MA, Kemerink, GJ, Pakbiers, MT, Heidendal, GA, Saris, WH 1994a. Beta-adrenergic stimulation of energy expenditure and forearm skeletal muscle metabolism in lean and obese men. American Journal of Physiology-Endocrinology and Metabolism 267, E306E315.CrossRefGoogle ScholarPubMed
Blaak, EE, Van Baak, MA, Kemerink, GJ, Pakbiers, MT, Heidendal, GA, Saris, WH 1994b. beta-Adrenergic stimulation of skeletal muscle metabolism in relation to weight reduction in obese men. American Journal of Physiology-Endocrinology and Metabolism 267, E316E322.CrossRefGoogle ScholarPubMed
Brennan, CL, Hoenig, M, Ferguson, DC 2004. GLUT4 but not GLUT1 expression decreases early in the development of feline obesity. Domestic Animal Endocrinology 26, 291301.CrossRefGoogle Scholar
Brown, M 2008. Skeletal muscle and bone: effect of sex steroids and aging. Advances in Physiology Education 32, 120126.CrossRefGoogle ScholarPubMed
Budde, EF 1952. The determination of fat in baked biscuit type of dog foods. Journal of the Association of Official Agricultural Chemists 35, 799805.Google Scholar
Cave, NJ, Backus, RC, Marks, SL, Klasing, KC 2007. Oestradiol and genistein reduce food intake in male and female overweight cats after gonadectomy. New Zealand Veterinary Journal 55, 113119.CrossRefGoogle ScholarPubMed
Cooke, PS, Naaz, A 2004. Role of estrogens in adipocyte development and function. Experimental Biology and Medicine 229, 11271135.CrossRefGoogle Scholar
Donoghue, S, Scarlett, JM 1998. Diet and feline obesity. Journal of Nutrition 128, 2776S2778S.CrossRefGoogle ScholarPubMed
Fettman, MJ, Stanton, CA, Banks, LL, Hamar, DW, Johnson, DE, Hegstad, RL, Johnston, S 1997. Effects of neutering on bodyweight, metabolic rate, and glucose tolerance of domestic cats. Research in Veterinary Science 62, 131136.CrossRefGoogle ScholarPubMed
Flynn, MF, Hardie, EM, Armstrong, PJ 1996. Effect of ovariohysterectomy on maintenance energy requirement in cats. Journal of the American Veterinary Medical Association 209, 15721581.CrossRefGoogle ScholarPubMed
Freeman, LM, Abood, SK, Fascetti, AJ, Fleeman, LM, Michel, KM, Laflamme, DP, Bauer, C, Kemp, BLE, Van Doren, JR, Willoughby, KN 2006. Disease prevalence among dogs and cats in the United States and Australia and proportion of dogs and cats that receive therapeutic diets or dietary supplements. Journal of the American Veterinary Medical Association 229, 531534.CrossRefGoogle ScholarPubMed
Garey, J, Morgan, MA, Frohlich, J, McEwen, BS, Pfaff, DW 2001. Effects of the phytoestrogen coumestrol on locomotor and fear-related behaviors in female mice. Hormones and Behavior 40, 6576.CrossRefGoogle ScholarPubMed
Harper, EJ, Stack, DM, Watson, TD, Moxham, G 2001. Effects of feeding regimens on bodyweight, composition and condition score in cats following ovariohysterectomy. Journal of Small Animal Practice 42, 433438.CrossRefGoogle ScholarPubMed
Hayes, MR, Miller, CK, Ulbrecht, JS, Mauger, JL, Parker-Klees, L, Davis Gutschall, M, Mitchell, DC, Smiciklas-Wright, H, Covasa, M 2007. A carbohydrate-restricted diet alters gut peptides and adiposity signals in men and women with metabolic syndrome. Journal of Nutrition 137, 19441950.CrossRefGoogle ScholarPubMed
Hoenig, M, McGoldrick, JB, deBeer, M, Demacker, PNM, Ferguson, DC 2006. Activity and tissue-specific expression of lipases and tumor-necrosis factor α in lean and obese cats. Domestic Animal Endocrinology 30, 333344.CrossRefGoogle ScholarPubMed
Hoenig, M, Thomaseth, K, Waldron, M, Ferguson, DC 2007. Insulin sensitivity, fat distribution, and adipocytokine response to different diets in lean and obese cats before and after weight loss. American Journal of Physiology 292, R227R234.Google ScholarPubMed
Kahn, BB, Pedersen, O 1993. Suppression of GLUT4 expression in skeletal muscle of rats that are obese from high fat feeding but not from high carbohydrate feeding or genetic obesity. Endocrinology 132, 1322.CrossRefGoogle ScholarPubMed
Kanchuk, ML, Backus, RC, Calvert, CC, Morris, JG, Rogers, QR 2003. Weight gain in gonadectomized normal and lipoprotein lipase-deficient male domestic cats results from increased food intake and not decreased energy expenditure. Journal of Nutrition 133, 18661874.CrossRefGoogle Scholar
Knerr, I, Herzog, D, Rauh, M, Rascher, W, Horbach, T 2006. Leptin and ghrelin expression in adipose tissues and serum levels in gastric banding patients. Europena Journal of Clinical Investigation 36, 389394.CrossRefGoogle ScholarPubMed
Laflamme, DP 1997. Development and validation of a body condition score system for cats: a clinical tool. Feline Practice 25, 1318.Google Scholar
Laflamme, DP, Hannah, SS 2005. Increased dietary protein promotes fat loss and reduces loss of lean body mass during weight loss in cats. International Journal of Applied Research in Veterinary Medicine 3, 6268.Google Scholar
Large, V, Reynisdottir, S, Langin, D, Fredby, K, Klannemark, M, Holm, C, Arner, P 1999. Decreased expression and function of adipocyte hormone-sensitive lipase in subcutaneous fat cells of obese subjects. Journal of Lipid Research 40, 20592065.CrossRefGoogle ScholarPubMed
Lejeune, MP, Westerterp, KR, Adam, TC, Luscombe-Marsh, ND, Westerterp-Plantenga, MP 2006. Ghrelin and glucagon-like peptide 1 concentrations, 24-h satiety, and energy and substrate metabolism during a high-protein diet and measured in a respiration chamber. American Journal of Clinical Nutrition 83, 8994.CrossRefGoogle Scholar
Liddle, RA, Green, GM, Conrad, CK, Williams, JA 1986. Proteins but not amino acids, carbohydrates, or fats stimulate cholecystokinin secretion in the rat. American Journal of Physiology 251, G243G248.Google ScholarPubMed
Lund, EM, Armstrong, PJ, Kirk, CA, Klausner, JS 2005. Prevalence and risk factors for obesity in adult cats from private US veterinary practices. International Journal of Applied Research in Veterinary Medicine 3, 8896.Google Scholar
Martin, L, Siliart, B, Dumon, H, Backus, R, Biourge, V, Nguyen, P 2001. Leptin, body fat content and energy expenditure in intact and gonadectomized adult cats: a preliminary study. Journal of Animal Physiology and Animal Nutrition 85, 195199.CrossRefGoogle ScholarPubMed
Meli, R, Pacilio, M, Raso, GM, Esposito, E, Coppola, A, Nasti, A, Di Carlo, C, Nappi, C, Di Carlo, R 2004. Estrogen and Raloxifene modulate leptin and its receptor in hypothalamus and adipose tissue from ovariectomized rats. Endocrinology 145, 31153121.CrossRefGoogle ScholarPubMed
Mystkowski, P, Schwartz, MW 2000. Gonadal steroids and energy homeostasis in the leptin era. Nutrition 16, 937946.CrossRefGoogle ScholarPubMed
Nguyen, PG, Dumon, HJ, Siliart, BS, Martin, LJ, Sergheraert, R, Biourge, VC 2004. Effects of dietary fat and energy on body weight and composition after gonadectomy in cats. American Journal of Veterinary Research 65, 17081713.CrossRefGoogle ScholarPubMed
National Research Council 2006. Nutrient requirements of dogs and cats. National Academies Press, Washington, DC, USA.Google Scholar
Prosky, L, Asp, NG, Schweizer, TF, DeVries, JW, Fruda, I 1992. Determination of insoluble and soluble dietary fiber in foods and food products: collaborative study. Journal of Association of Official Analytical Chemists International 75, 360367.Google Scholar
Robertson, ID 1999. The influence of diet and other factors on owner-perceived obesity in privately owned cats from metropolitan Perth, Western Australia. Preventive Veterinary Medicine 40, 7585.CrossRefGoogle ScholarPubMed
Root, MV, Johnston, SD, Olson, PN 1996. Effect of prepuberal and postpuberal gonadectomy on heat production measured by indirect calorimetry in male and female domestic cats. American Journal of Veterinary Research 57, 371374.CrossRefGoogle ScholarPubMed
Rotter, V, Nagaev, I, Smith, U 2003. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-α, overexpressed in human fat cells from insulin-resistant subjects. Journal of Biological Chemistry 278, 4577745784.CrossRefGoogle ScholarPubMed
Scarlett, JM, Donoghue, S, Saidla, J, Wills, J 1994. Overweight cats: prevalence and risk factors. International Journal of Obesity and Related Metabolic Disorders 18, S22S28.Google ScholarPubMed
Speakman, JR, Booles, D, Butterwick, R 2001. Validation of dual energy X-ray absorptiometry (DXA) by comparison with chemical analysis of dogs and cats. International Journal Obesity and Related Metabolic Disorders 25, 439447.CrossRefGoogle ScholarPubMed
Szabo, J, Ibrahim, WH, Sunvold, GD, Dickey, KM, Rodgers, JB, Toth, IE, Boissonneault, GA, Bruckner, GG 2000. Influence of dietary protein and lipid on weight loss in obese ovariohysterectomized cats. American Journal of Veterinary Research 61, 559565.CrossRefGoogle ScholarPubMed
Tanner, AE, Martin, J, Saker, KE 2007. Oxidative stress and inflammatory state induced by obesity in the healthy feline. Journal of Animal Physiology and Animal Nutrition 91, 163166.CrossRefGoogle Scholar
Tou, JCL, Wade, CE 2002. Determinants affecting physical activity levels in animal models. Experimental Biology and Medicine 227, 587600.CrossRefGoogle ScholarPubMed
Wade, GN, Gray, JM 1979. Gonadal effects on food intake and adiposity: a metabolic hypothesis. Physiology & Behavior 22, 583593.CrossRefGoogle ScholarPubMed
Zini, E, Linscheid, P, Franchini, M, Kaufmann, K, Monnais, E, Kutter, AP, Ackermann, M, Lutz, TA, Reusch, CE 2009. Partial sequencing and expression of genes involved in glucose metabolism in adipose tissues and skeletal muscle of healthy cats. Veterinary Journal 180, 6670.CrossRefGoogle ScholarPubMed