Obesity: the protein leverage hypothesis
SJ Simpson, Department of Zoology and University Museum of Natural History, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK. E‐mail: stephen.simpson@zoo.ox.ac.uk; D Raubenheimer, School of Biological Sciences and Psychology Department, University of Auckland, New Zealand, Private Bag 92019, Auckland, New Zealand. E‐mail: david.raubenheimer@auckland.ac.nz
Summary
The obesity epidemic is among the greatest public health challenges facing the modern world. Regarding dietary causes, most emphasis has been on changing patterns of fat and carbohydrate consumption. In contrast, the role of protein has largely been ignored, because (i) it typically comprises only ∼15% of dietary energy, and (ii) protein intake has remained near constant within and across populations throughout the development of the obesity epidemic. We show that, paradoxically, these are precisely the two conditions that potentially provide protein with the leverage both to drive the obesity epidemic through its effects on food intake, and perhaps to assuage it. We formalize this hypothesis in a mathematical model. Some supporting epidemiological, experimental and animal data are presented, and predictions are made for future testing.
Citing Literature
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- Caley A. Johnson, David Raubenheimer, Jessica M. Rothman, David Clarke, Larissa Swedell and Tobias Deschner, 30 Days in the Life: Daily Nutrient Balancing in a Wild Chacma Baboon, PLoS ONE, 8, 7, (e70383), (2013).
- Kim Jensen, Sabine Engelke, Stephen J. Simpson, David Mayntz and John Hunt, Balancing of specific nutrients and subsequent growth and body composition in the slug Arion lusitanicus, Physiology & Behavior, 122, (84), (2013).
- Benjamin G. Fanson, Ingrid E. Petterson and Phillip W. Taylor, Diet quality mediates activity patterns in adult Queensland fruit fly (Bactrocera tryoni), Journal of Insect Physiology, 59, 7, (676), (2013).
- Xin Huang, Dale P. Hancock, Alison K. Gosby, Aisling C. McMahon, Samantha M.C. Solon, David G. Le Couteur, Arthur D. Conigrave, David Raubenheimer and Stephen J. Simpson, Effects of dietary protein to carbohydrate balance on energy intake, fat storage, and heat production in mice, Obesity, 21, 1, (85-92), (2013).
- Haitao Zhao, Xiaowei Wang, Brigitte Kreigenhofer, Xiaoguang Qi, Songtao Guo, Chengliang Wang, Jian Zhang, Jianqiang Zhao and Baoguo Li, Study on the nutritional ecology of wild primates, Acta Ecologica Sinica, 33, 4, (185), (2013).
- Alison K. Gosby, Arthur D. Conigrave, David Raubenheimer and Stephen J. Simpson, Protein leverage and energy intake, Obesity Research & Clinical Practice, 7, (e110), (2013).
- Tracy G. Anthony, Christopher D. Morrison and Thomas W. Gettys, Remodeling of Lipid Metabolism by Dietary Restriction of Essential Amino Acids, Diabetes, 62, 8, (2635), (2013).
- Sarah I. Martire, Nathan Holmes, R. Fred Westbrook, Margaret J. Morris and Mihai Covasa, Altered Feeding Patterns in Rats Exposed to a Palatable Cafeteria Diet: Increased Snacking and Its Implications for Development of Obesity, PLoS ONE, 8, 4, (e60407), (2013).
- Adrian K. Hewson-Hughes, Victoria L. Hewson-Hughes, Alison Colyer, Andrew T. Miller, Scott J. McGrane, Simon R. Hall, Richard F. Butterwick, Stephen J. Simpson and David Raubenheimer, Geometric analysis of macronutrient selection in breeds of the domestic dog, Canis lupus familiaris, Behavioral Ecology, 24, 1, (293), (2013).
- G. Keith Harris and E. Allen Foegeding, Protein‐Based Designs for Healthier Foods of the Future, Formulation Engineering of Foods, (9-43), (2013).
- Francisco Catanese, Marianela Obelar, Juan J. Villalba and Roberto A. Distel, The importance of diet choice on stress-related responses by lambs, Applied Animal Behaviour Science, 148, 1-2, (37), (2013).
- O Davidenko, N Darcel, G Fromentin and D Tomé, Control of protein and energy intake - brain mechanisms, European Journal of Clinical Nutrition, 67, 5, (455), (2013).
- Helen O'Connor, The Overweight Athlete, The Encyclopaedia of Sports Medicine, (503-512), (2013).
- Ramesh Sahani, Foraging to settled life: A comparative study of anthropometry and nutrition of Onges of Little Andaman Island, HOMO, 10.1016/j.jchb.2013.07.003, 64, 5, (391-397), (2013).
- Éric Le Bourg, Restriction de nourriture, longévité et vieillissement, Cahiers de Nutrition et de Diététique, 47, 2, (85), (2012).
- Kari Britt Schroeder, Book Review, Evolution and Human Behavior, 33, 2, (165), (2012).
- Regina Belski, Fiber, Protein, and Lupin-Enriched Foods: Role for Improving Cardiovascular Health, Advances in Food and Nutrition Research Volume 66, 10.1016/B978-0-12-394597-6.00004-5, (147-215), (2012).
- Éric Le Bourg, Dietary Restriction Studies in Humans: Focusing on Obesity, Forgetting Longevity, Gerontology, 58, 2, (126), (2012).
- Andreu Nubiola and Imma Remolins, Dieta hipoglucídica en el tratamiento de la diabetes tipo 2, Avances en Diabetología, 28, 6, (131), (2012).
- Hans-Rudolf Berthoud, Heike Münzberg, Brenda K. Richards and Christopher D. Morrison, Neural and metabolic regulation of macronutrient intake and selection, Proceedings of the Nutrition Society, 71, 03, (390), (2012).
- Christopher D. Morrison, Scott D. Reed and Tara M. Henagan, Homeostatic regulation of protein intake: in search of a mechanism, American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 302, 8, (R917), (2012).
- D. Raubenheimer, S. J. Simpson and A. H. Tait, Match and mismatch: conservation physiology, nutritional ecology and the timescales of biological adaptation, Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 1596, (1628), (2012).
- Daniel J. Hruschka, Do economic constraints on food choice make people fat? A critical review of two hypotheses for the poverty–obesity paradox, American Journal of Human Biology, 24, 3, (277-285), (2012).
- S. Y. Bai, D. I. Briggs and M. H. Vickers, Increased systolic blood pressure in rat offspring following a maternal low-protein diet is normalized by maternal dietary choline supplementation, Journal of Developmental Origins of Health and Disease, 3, 05, (342), (2012).
- Sanne Griffioen-Roose, Monica Mars, Els Siebelink, Graham Finlayson, Daniel Tomé and Cees de Graaf, Protein status elicits compensatory changes in food intake and food preferences, The American Journal of Clinical Nutrition, 95, 1, (32), (2012).
- Jennie C. Brand-Miller, Hayley J. Griffin and Stephen Colagiuri, The Carnivore Connection Hypothesis: Revisited, Journal of Obesity, 2012, (1), (2012).
- Michelle Blumfield, Alexis Hure, Lesley MacDonald-Wicks, Roger Smith, Stephen Simpson, David Raubenheimer and Clare Collins, The Association between the Macronutrient Content of Maternal Diet and the Adequacy of Micronutrients during Pregnancy in the Women and Their Children’s Health (WATCH) Study, Nutrients, 4, 12, (1958), (2012).
- Sanne Griffioen-Roose, Pleunie S. Hogenkamp, Monica Mars, Graham Finlayson and Cees de Graaf, Taste of a 24-h diet and its effect on subsequent food preferences and satiety, Appetite, 59, 1, (1), (2012).
- A. K. Portella, E. Kajantie, P. Hovi, M. Desai, M. G. Ross, M. Z. Goldani, T. J. Roseboom and P. P. Silveira, Effects of in utero conditions on adult feeding preferences, Journal of Developmental Origins of Health and Disease, 3, 03, (140), (2012).
- B. L. Heitmann, K. R. Westerterp, R. J. F. Loos, T. I. A. Sørensen, K. O'Dea, P. McLean, T. K. Jensen, J. Eisenmann, J. R. Speakman, S. J. Simpson, D. R. Reed and M. S. Westerterp-Plantenga, Obesity: lessons from evolution and the environment, Obesity Reviews, 13, 10, (910), (2012).
- Michelle L Blumfield, Alexis J Hure, Lesley K MacDonald-Wicks, Roger Smith, Stephen J Simpson, Warwick B Giles, David Raubenheimer and Clare E Collins, Dietary balance during pregnancy is associated with fetal adiposity and fat distribution, The American Journal of Clinical Nutrition, 96, 5, (1032), (2012).
- Angela Köhler, David Raubenheimer and Susan W. Nicolson, Regulation of nutrient intake in nectar-feeding birds: insights from the geometric framework, Journal of Comparative Physiology B, 182, 5, (603), (2012).
- Claudia Martinez-Cordero, Christopher W. Kuzawa, Deborah M. Sloboda, Joanna Stewart, Stephen J. Simpson and David Raubenheimer, Testing the Protein Leverage Hypothesis in a free-living human population, Appetite, 59, 2, (312), (2012).
- Sanne Griffioen-Roose, Monica Mars, Graham Finlayson, John E. Blundell and Cees de Graaf, The effect of within-meal protein content and taste on subsequent food choice and satiety, British Journal of Nutrition, 106, 05, (779), (2011).
- Shawn M. Wilder, Spider Nutrition, Spider Physiology and Behaviour - Physiology, 10.1016/B978-0-12-387668-3.00002-7, (87-136), (2011).
- F L Garden, G B Marks, C Almqvist, J M Simpson and K L Webb, Infant and early childhood dietary predictors of overweight at age 8 years in the CAPS population, European Journal of Clinical Nutrition, 65, 4, (454), (2011).
- Emma N. Bermingham, Sandra Kittelmann, Gemma Henderson, Wayne Young, Nicole C. Roy and David G. Thomas, Five-week dietary exposure to dry diets alters the faecal bacterial populations in the domestic cat (Felis catus), British Journal of Nutrition, 106, S1, (S49), (2011).
- George Bray, References, A Guide to Obesity and the Metabolic Syndrome, 10.1201/b10790-15, (283-360), (2011).
- Stephen J. Simpson and David Raubenheimer, The nature of nutrition: a unifying framework, Australian Journal of Zoology, 59, 6, (350), (2011).
- Alasdair I. Houston, Andrew D. Higginson and John M. McNamara, Optimal foraging for multiple nutrients in an unpredictable environment, Ecology Letters, 14, 11, (1101-1107), (2011).
- Stijn Soenen, Ananda Hochstenbach‐Waelen and Margriet S. Westerterp‐Plantenga, Efficacy of α‐Lactalbumin and Milk Protein on Weight Loss and Body Composition During Energy Restriction, Obesity, 19, 2, (370-379), (2012).
- Helen O'Connor and Gary Slater, Losing, Gaining and Making Weight for Athletes, Sport and Exercise Nutrition, (210-232), (2011).
- Alex R. Kraaijeveld, Naji P. Elrayes, Hansjürgen Schuppe and Philip L. Newland, l-Arginine enhances immunity to parasitoids in Drosophila melanogaster and increases NO production in lamellocytes, Developmental & Comparative Immunology, 10.1016/j.dci.2011.03.019, 35, 8, (857-864), (2011).
- Ashley J.W. Ward, James E. Herbert-Read and Stephen J. Simpson, Diets and decisions: the potential use of food protein cues in dietary, sexual and social decisions by mosquitofish, Animal Behaviour, 82, 4, (783), (2011).
- Reinald Pamplona and Gustavo Barja, An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeotherms, Biogerontology, 10.1007/s10522-011-9348-1, 12, 5, (409-435), (2011).
- Ananda Hochstenbach-Waelen, Stijn Soenen, Klaas R. Westerterp and Margriet S. Westerterp-Plantenga, Effects of a supra-sustained gelatin–milk protein diet compared with (supra-)sustained milk protein diets on body-weight loss, British Journal of Nutrition, 105, 09, (1388), (2011).
- Misha A. Vargas, Ningguang Luo, Atsushi Yamaguchi and Pankaj Kapahi, A Role for S6 Kinase and Serotonin in Postmating Dietary Switch and Balance of Nutrients in D. melanogaster, Current Biology, 20, 11, (1006), (2010).
- Allan Sørensen, David Mayntz, Stephen James Simpson and David Raubenheimer, Dietary ratio of protein to carbohydrate induces plastic responses in the gastrointestinal tract of mice, Journal of Comparative Physiology B, 180, 2, (259), (2010).
- Alison K. Gosby, Suzanne Soares-Wynter, Claudia Campbell, Asha Badaloo, Marion Antonelli, Rosemary M. Hall, Claudia Martinez-Cordero, Susan A. Jebb, Jennie Brand-Miller, Ian D. Caterson, Arthur D. Conigrave, Terrence G. Forrester, David Raubenheimer and Stephen J. Simpson, Design and testing of foods differing in protein to energy ratios, Appetite, 55, 2, (367), (2010).
- Robert Brooks, Alexei Maklakov and Daniel J. Rankin, Sex Differences in Obesity Associated with Total Fertility Rate, PLoS ONE, 5, 5, (e10587), (2010).
- M. Kearney, S. J. Simpson, D. Raubenheimer and B. Helmuth, Modelling the ecological niche from functional traits, Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 1557, (3469), (2010).
- Paul A. M. Smeets, Dietary learning: both consistency and congruency matter, Nature Reviews Endocrinology, 6, 8, (1), (2010).
- E L K Mortensen, T Wang, H Malte, D Raubenheimer and D Mayntz, Maternal preconceptional nutrition leads to variable fat deposition and gut dimensions of adult offspring mice (C57BL/6JBom), International Journal of Obesity, 34, 11, (1618), (2010).
- Kim Jensen, David Mayntz, Tobias Wang, Stephen J. Simpson and Johannes Overgaard, Metabolic consequences of feeding and fasting on nutritionally different diets in the wolf spider Pardosa prativaga, Journal of Insect Physiology, 56, 9, (1095), (2010).
- S. SISODIA and B. N. SINGH, Resistance to environmental stress in Drosophila ananassae: latitudinal variation and adaptation among populations, Journal of Evolutionary Biology, 23, 9, (1979-1988), (2010).
- R. C. Brooks, S. J. Simpson and D. Raubenheimer, The price of protein: combining evolutionary and economic analysis to understand excessive energy consumption, Obesity Reviews, 11, 12, (887-894), (2010).
- Sanne Griffioen-Roose, Graham Finlayson, Monica Mars, John E. Blundell and Cees de Graaf, Measuring food reward and the transfer effect of sensory specific satiety, Appetite, 55, 3, (648), (2010).
- James M. Shikany, Laura K. Vaughan, Monica L. Baskin, Mark B. Cope, James O. Hill and David B. Allison, Is Dietary Fat “Fattening”? A Comprehensive Research Synthesis, Critical Reviews in Food Science and Nutrition, 50, 8, (699), (2010).
- Antti Kause, Cheryl D. Quinton, Kari Ruohonen and Juha Koskela, Genetic potential for the regulation of variability in body lipid and protein content of European whitefish (Coregonus lavaretus), British Journal of Nutrition, 101, 10, (1444), (2009).
- Antti Forsman and Kari Ruohonen, Dynamics of protein and lipid intake regulation of rainbow trout studied with a wide lipid range of encapsulated diets and self-feeders, Physiology & Behavior, 96, 1, (85), (2009).
- Spencer T. Behmer, Insect Herbivore Nutrient Regulation, Annual Review of Entomology, 54, 1, (165), (2009).
- A-M Paradis, G Godin, L Pérusse and M-C Vohl, Associations between dietary patterns and obesity phenotypes, International Journal of Obesity, 33, 12, (1419), (2009).
- Brittany M. Vester, Kari J. Liu, Tonya L. Keel, Thomas K. Graves and Kelly S. Swanson, In utero and postnatal exposure to a high-protein or high-carbohydrate diet leads to differences in adipose tissue mRNA expression and blood metabolites in kittens, British Journal of Nutrition, 102, 08, (1136), (2009).
- Annika M. Felton, Adam Felton, Jeff T. Wood, William J. Foley, David Raubenheimer, Ian R. Wallis and David B. Lindenmayer, Nutritional Ecology of Ateles chamek in lowland Bolivia: How Macronutrient Balancing Influences Food Choices, International Journal of Primatology, 30, 5, (675), (2009).
- James Warbrick‐Smith, David Raubenheimer, Stephen J. Simpson and Spencer T. Behmer, Three hundred and fifty generations of extreme food specialisation: testing predictions of nutritional ecology, Entomologia Experimentalis et Applicata, 132, 1, (65-75), (2009).
- Annika M. Felton, Adam Felton, David B. Lindenmayer and William J. Foley, Nutritional goals of wild primates, Functional Ecology, 23, 1, (70-78), (2009).
- David Raubenheimer, Steven J. Simpson and David Mayntz, Nutrition, ecology and nutritional ecology: toward an integrated framework, Functional Ecology, 23, 1, (4-16), (2009).
- Annika M. Felton, Adam Felton, David Raubenheimer, Stephen J. Simpson, William J. Foley, Jeff T. Wood, Ian R. Wallis and David B. Lindenmayer, Protein content of diets dictates the daily energy intake of a free-ranging primate, Behavioral Ecology, 20, 4, (685), (2009).
- David Mayntz, Vivi Hunnicke Nielsen, Allan Sørensen, Søren Toft, David Raubenheimer, Carsten Hejlesen and Stephen James Simpson, Balancing of protein and lipid intake by a mammalian carnivore, the mink, Mustela vison, Animal Behaviour, 77, 2, (349), (2009).
- Marion Le Rohellec and Éric Le Bourg, Contrasted effects of suppressing live yeast from food on longevity, aging and resistance to several stresses in Drosophila melanogaster, Experimental Gerontology, 44, 11, (695), (2009).
- Ken Cheng, Stephen J. Simpson and David Raubenheimer, A Geometry of Regulatory Scaling, The American Naturalist, 172, 5, (681), (2008).
- Danielle A. Skorupa, Azra Dervisefendic, Jessica Zwiener and Scott D. Pletcher, Dietary composition specifies consumption, obesity, and lifespan in Drosophila melanogaster, Aging Cell, 7, 4, (478-490), (2008).
- Allan Sørensen, David Mayntz, David Raubenheimer and Stephen J. Simpson, Protein‐leverage in Mice: The Geometry of Macronutrient Balancing and Consequences for Fat Deposition, Obesity, 16, 3, (566-571), (2012).
- Gaynor Heading, Rural obesity, healthy weight and perceptions of risk: Struggles, strategies and motivation for change, Australian Journal of Rural Health, 16, 2, (86-91), (2008).
- P. L. Newland and P. Yates, Nitric Oxide Modulates Salt and Sugar Responses via Different Signaling Pathways, Chemical Senses, 10.1093/chemse/bjm094, 33, 4, (347-356), (2008).
- J. William O. Ballard, R.G. Melvin and S.J. Simpson, Starvation resistance is positively correlated with body lipid proportion in five wild caught Drosophila simulans populations, Journal of Insect Physiology, 54, 9, (1371), (2008).
- Charles T. Robbins, Jennifer K. Fortin, Karyn D. Rode, Sean D. Farley, Lisa A. Shipley and Laura A. Felicetti, Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore, Oikos, 116, 10, (1675-1682), (2007).
- S. A. Jebb, Dietary determinants of obesity, Obesity Reviews, 8, (93-97), (2007).
- D. Canoy and I. Buchan, Challenges in obesity epidemiology, Obesity Reviews, 8, (1-11), (2007).
- D.J. Mela, Liking, wanting and eating: drivers of food choice and intake in obesity11.This chapter is an extended version of Mela DJ (2006), ‘Eating for pleasure or just wanting to eat? Reconsidering sensory hedonic responses as a driver of obesity’, Appetite, 47(1), 10–17. Extensive use is made of the original text and figures, with permission of the publishers., Understanding Consumers of Food Products, 10.1533/9781845692506.4.393, (393-411), (2007).
- Garden Tabacchi, Santo Giammanco, Maurizio La Guardia and Marco Giammanco, A review of the literature and a new classification of the early determinants of childhood obesity: from pregnancy to the first years of life, Nutrition Research, 27, 10, (587), (2007).
- Charles T. Robbins, Jennifer K. Fortin, Karyn D. Rode, Sean D. Farley, Lisa A. Shipley and Laura A. Felicetti, Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore, Oikos, 116, 10, (1675), (2007).
- S. J. Simpson and D. Raubenheimer, Caloric Restriction and Aging Revisited: The Need for a Geometric Analysis of the Nutritional Bases of Aging, The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 62, 7, (707), (2007).
- Kari Ruohonen, Stephen J. Simpson and David Raubenheimer, A new approach to diet optimisation: A re-analysis using European whitefish (Coregonus lavaretus), Aquaculture, 267, 1-4, (147), (2007).
- P. D. Gluckman and M. A. Hanson, Developmental plasticity and human disease: research directions, Journal of Internal Medicine, 261, 5, (461-471), (2007).
- Manny NOAKES, Jennifer KEOGH and Peter CLIFTON, Obesity and type 2 diabetes mellitus, Nutrition & Dietetics, 64, (S156-S161), (2007).
- E.L. Gibson and J.M. Brunstrom, Learned Influences on Appetite, Food Choice, and Intake, Appetite and Body Weight, 10.1016/B978-012370633-1/50011-6, (271-300), (2007).
- J. Warbrick-Smith, S. T. Behmer, K. P. Lee, D. Raubenheimer and S. J. Simpson, Evolving resistance to obesity in an insect, Proceedings of the National Academy of Sciences, 103, 38, (14045), (2006).
- David J. Mela, Eating for pleasure or just wanting to eat? Reconsidering sensory hedonic responses as a driver of obesity, Appetite, 47, 1, (10), (2006).
- A Astrup, Carbohydrates as macronutrients in relation to protein and fat for body weight control, International Journal of Obesity, 30, S3, (S4), (2006).
- Maarten Boersma and James J. Elser, TOO MUCH OF A GOOD THING: ON STOICHIOMETRICALLY BALANCED DIETS AND MAXIMAL GROWTH, Ecology, 87, 5, (1325-1330), (2006).
- D Raubenheimer, K.P Lee and S.J Simpson, Does Bertrand's rule apply to macronutrients?, Proceedings of the Royal Society B: Biological Sciences, 272, 1579, (2429), (2005).
- Ali Khoddami, Peter V. Chrystal, Peter H. Selle and Sonia Yun Liu, Dietary starch to lipid ratios influence growth performance, nutrient utilisation and carcass traits in broiler chickens offered diets with different energy densities, PLOS ONE, 10.1371/journal.pone.0205272, 13, 10, (e0205272), (2018).
- Ekhlas Al Shareefi and Sheena C Cotter, The nutritional ecology of maturation in a carnivorous insect, Behavioral Ecology, 10.1093/beheco/ary142, (2018).
- Letícia Barbosa Gabriel da Silva, Eliane Lopes Rosado, Patricia de Carvalho Padilha, Juliana Rebelo Dias, Tainá Marques Moreira, Tatiana Pereira de Paula, Denise Cavalcante de Barros and Cláudia Saunders, Food intake of women with gestational diabetes mellitus, in accordance with two methods of dietary guidance: a randomised controlled clinical trial, British Journal of Nutrition, 10.1017/S0007114518001484, (1-11), (2018).
- David Allaway, Carlos H. de Alvaro, Adrian Hewson-Hughes, Ruth Staunton, Penelope Morris and Janet Alexander, Impact of dietary macronutrient profile on feline body weight is not consistent with the protein leverage hypothesis, British Journal of Nutrition, 10.1017/S000711451800257X, (1-9), (2018).
- J. S. Forbey, R. Liu, T. T. Caughlin, M. D. Matocq, J. A. Vucetich, K. D. Kohl, M. D. Dearing and A. M. Felton, Review: Using physiologically based models to predict population responses to phytochemicals by wild vertebrate herbivores, animal, 10.1017/S1751731118002264, (1-16), (2018).
