Chowing down: diet considerations in rodent models of metabolic disease

Abstract

Diet plays a substantial role in the etiology, progression, and treatment of chronic disease and is best considered as a multifaceted set of modifiable input variables with pleiotropic effects on a variety of biological pathways spanning multiple organ systems. This brief review discusses key issues related to the design and conduct of diet interventions in rodent models of metabolic disease and their implications for interpreting experiments. We also make specific recommendations to improve rodent diet studies to help better understand the role of diet on metabolic physiology and thereby improve our understanding of metabolic disease.

Keywords

diet composition / nutrition / chow / study design / recommendations

References

[1] Hitchcock CR , Bell ET . Studies on the nematode parasite, Gongylonema neoplasticum (spiroptera neoplasticum), and avitaminosis A in the forestomach of rats: comparison with Fibiger’s results. J Natl Cancer Inst 1952; 12: 1345- 87.

[2] Erling Norrby. Nobel Prizes and Life Sciences. London and Singapore: World Scientific Press, 2010.

[3] Council, National Research. Nutrient Requirements of Laboratory Animals: Cat, Guinea Pig, Hamster, Monkey, Mouse, Rat (2nd Revised edn). Washington, DC: The National Academies Press, 1972.

[4] Knapka JJ , Smith KP , Judge FJ . Effect of open and closed formula rations on the performance of three strains of laboratory mice. Lab Anim Sci 1974; 24: 480- 7.

[5] Rao GN . New diet (NTP-2000) for rats in the National Toxicology Program toxicity and carcinogenicity studies. Fundam Appl Toxicol 1996; 32: 102- 8.

[6] Reeves PG , Nielsen FH , Fahey GC Jr . AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 199; 123: 1939- 51.

[7] Rees ML , Gioscia-Ryan RA , McCune SA et al. The AIN-76A defined rodent diet accelerates the development of heart failure in SHHF rats: a cautionary note on its use in cardiac studies. J Anim Physiol Anim Nutr (Berl) 2014; 98: 56- 64.

[8] Diet, Nutrition and the Prevention of Chronic Diseases. Geneva, Switzerland: World Health Organization technical report series 2003. 916: i-viii, 1-149, backcover,

[9] NationalAcademies of Sciences, Engineering, and Medicine, Health and Medicine Division, Food and Nutrition Board, and Committee on the Development of Guiding Principles for the Inclusion of Chronic Disease Endpoints in Future Dietary Reference Intakes. Guiding Principles for Developing Dietary Reference Intakes Based on Chronic Disease. Maria P. Oria, Shiriki Kumanyika (ed.). Washington, DC: National Academies Press (US), 2017.

[10] Warden CH , Fisler JS . Comparisons of diets used in animal models of high-fat feeding. Cell Metab 2008; 7: 277.

[11] Pellizzon MA , Ricci MR . The common use of improper control diets in diet-induced metabolic disease research confounds data interpretation: the fiber factor. Nutr Metab (Lond) 2018; 15: 3.

[12] Tuck CJ , De Palma G , Takami K et al. Nutritional profile of rodent diets impacts experimental reproducibility in microbiome preclinical research. Sci Rep 2020; 10: 17784.

[13] Pellizzon MA , Ricci MR . Choice of laboratory rodent diet may confound data interpretation and reproducibility. Curr Dev Nutr 2020; 4: nzaa031.

[14] Greenman DL , Oller WL , Littlefield NA et al. Commercial laboratory animal diets: toxicant and nutrient variability. J Toxicol Environ Health 1980; 6: 235- 46.

[15] Wise A , Gilburt DJ . The variability of dietary fibre in laboratory animal diets and its relevance to the control of experimental conditions. Food Cosmet Toxicol 1980; 18: 643- 8.

[16] Newberne PM , Fox JG . Nutritional adequacy and quality control of rodent diets. Lab Anim Sci 1980; 30: 352- 65.

[17] Newberne PM , Sotnikov AV . Diet: the neglected variable in chemical safety evaluations. Toxicol Pathol 1996; 24: 746- 56.

[18] Liu R , Cheng M , Kothapalli KSD et al. Glycerol derived process contaminants in refined coconut oil induce cholesterol synthesis in HepG2 cells. Food Chem Toxicol 2019; 127: 135- 42.

[19] Turnbaugh PJ , Ley RE , Mahowald MA et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027- 31.

[20] Ley RE , Bäckhed F , Turnbaugh P et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 2005; 102: 11070- 5.

[21] Turnbaugh PJ , Bäckhed F , Fulton L et al. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008; 3: 213- 23.

[22] Dalby MJ , Ross AW , Walker AW et al. Dietary uncoupling of gut microbiota and energy harvesting from obesity and glucose tolerance in mice. Cell Rep 2017; 21: 1521- 33.

[23] Ables GP , Perrone CE , Orentreich D et al. Methionine-restricted C57BL/6J mice are resistant to diet-induced obesity and insulin resistance but have low bone density. PLoS One 2012; 7: e51357.

[24] Plaisance EP , Henagan TM , Echlin H et al. Role of β-adrenergic receptors in the hyperphagic and hypermetabolic responses to dietary methionine restriction. Am J Physiol Regul Integr Comp Physiol 2010; 299: R740- 50.

[25] Hasek BE , Stewart LK , Henagan TM et al. Dietary methionine restriction enhances metabolic flexibility and increases uncoupled respiration in both fed and fasted states. Am J Physiol Regul Integr Comp Physiol 2010; 299: R728- 39.

[26] Zhang X , Sergin I , Evans TD et al. High-protein diets increase cardiovascular risk by activating macrophage mTOR to suppress mitophagy. Nat Metab 2020; 2: 110- 25.

[27] Simpson SJ , Le Couteur DG , James DE et al. The Geometric Framework for Nutrition as a tool in precision medicine. Nutr Healthy Aging 2017; 4: 217- 26.

[28] Solon-Biet SM , McMahon AC , Ballard JW et al. The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. Cell Metab 2014; 19: 418- 30.

[29] Solon-Biet SM , Mitchell SJ , Coogan SC et al. Dietary protein to carbohydrate ratio and caloric restriction: comparing metabolic outcomes in mice. Cell Rep 2015; 11: 1529- 34.

[30] Solon-Biet SM , Walters KA , Simanainen UK et al. Macronutrient balance, reproductive function, and lifespan in aging mice. Proc Natl Acad Sci U S A 2015; 112: 3481- 6.

[31] Hu S , Wang L , Yang D et al. Dietary fat, but not protein or carbohydrate, regulates energy intake and causes adiposity in mice. Cell Metab 2018; 28: 415- 31.e4.

[32] Hu S , Togo J , Wang L et al. Effects of dietary macronutrients and body composition on glucose homeostasis in mice. Natl Sci Rev 2020; 8: nwaa177.

[33] Cameron KM , Speakman JR . The extent and function of ‘food grinding’ in the laboratory mouse (Mus musculus). Lab Anim 2010; 44: 298- 304.

[34] Król E , Duncan JS , Redman P et al. Photoperiod regulates leptin sensitivity in field voles, Microtus agrestis. J Comp Physiol B 2006; 176: 153- 63.

[35] Król E , Redman P , Thomson PJ et al. Effect of photoperiod on body mass, food intake and body composition in the field vole, Microtus agrestis. J Exp Biol 2005; 208: 571- 84.

[36] Giovannetti PM . Effect of coprophagy on nutrition. Nutr Res 1982; 2: 335- 49.

[37] Giovannetti PM , Stothers SC , Parker RJ . Coprophagy prevention and availability of amino acid in wheat for the growing rat. Can J Anim Sci 1970; 50: 269- 77.

[38] Barnes RH , Fiala G , McGehee B et al. Prevention of coprophagy in the rat. J Nutr 1957; 63: 489- 98.

[39] Bo TB , Zhang XY , Kohl KD et al. Coprophagy prevention alters microbiome, metabolism, neurochemistry, and cognitive behavior in a small mammal. ISME J 2020; 14: 2625- 45.

[40] Bogatyrev SR , Rolando JC , Ismagilov RF . Self-reinoculation with fecal flora changes microbiota density and composition leading to an altered bile-acid profile in the mouse small intestine. Microbiome 2020; 8: 19.

[41] Ambery AG , Tackett L , Penque BA et al. Effect of corncob bedding on feed conversion efficiency in a high-fat diet-induced prediabetic model in C57Bl/6J mice. J Am Assoc Lab Anim Sci 2014; 53: 449- 51.

[42] Gregor A , Fragner L , Trajanoski S et al. Cage bedding modifies metabolic and gut microbiota profiles in mouse studies applying dietary restriction. Sci Rep 2020; 10: 20835.

[43] Pak HH , Haws SA , Green CL et al. Fasting drives the metabolic, molecular and geroprotective effects of a calorie-restricted diet in mice. Nat Metab 2021; 3: 1327- 41.

[44] Donner A , Klar N . Pitfalls of and controversies in cluster randomization trials. Am J Public Health 2004; 94: 416- 22.

[45] Vorland CJ , Brown AW , Dawson JA et al. Errors in the implementation, analysis, and reporting of randomization within obesity and nutrition research: a guide to their avoidance. Int J Obes (Lond) 2021; 45: 2335- 46.

[46] Zhang LN , Morgan DG , Clapham JC et al. Factors predicting non-genetic variability in body weight gain induced by a high-fat diet in inbred C57BL/6J mice. Obesity (Silver Spring) 2012; 20: 1179- 88.

[47] Selimkhanov J , Thompson WC , Patterson TA et al. Evaluation of a mathematical model of rat body weight regulation in application to caloric restriction and drug treatment studies. PLoS One 2016; 11: e0155674.

[48] Fischer J , Koch L , Emmerling C et al. Inactivation of the FTO gene protects from obesity. Nature 2009; 458: 894- 8.

[49] Speakman JR . FTO effect on energy demand versus food intake. Nature 2010; 464: E1. discussion E2.

[50] Wu Y , Hu S , Yang D et al. Increased variation in body weight and food intake is related to increased dietary fat but not increased carbohydrate or protein in mice. Front Nutr 2022; 9: 835536.

[51] Guo J , Jou W , Gavrilova O et al. Persistent diet-induced obesity in male C57BL/6 mice resulting from temporary obesigenic diets. PLoS One 2009; 4: e5370.

[52] Sørensen A , Mayntz D , Raubenheimer D et al. Protein-leverage in mice: the geometry of macronutrient balancing and consequences for fat deposition. Obesity (Silver Spring) 2008; 16: 566- 71.

[53] Hughes RN . Sex still matters: has the prevalence of male-only studies of drug effects on rodent behaviour changed during the past decade? Behav Pharmacol 2019; 30: 95- 9.

[54] Takahashi A . Toward understanding the sex differences in the biological mechanism of social stress in mouse models. Front Psychiatry 2021; 12: 644161.

[55] National Research Council (US) Subcommittee on Laboratory Animal Nutrition. Nutrient Requirements of Laboratory Animals (4th Revised edn). Washington, DC: National Academies Press (US), 1995.

[56] Barrington WT , Wulfridge P , Wells AE et al. Improving metabolic health through precision dietetics in mice. Genetics 2018; 208: 399- 417.

RIGHTS & PERMISSIONS

The Author(s) 2023. Published by Oxford University Press on behalf of Higher Education Press.