The impact of caloric and non-caloric sweeteners on food intake and brain responses to food: A randomized crossover controlled trial in healthy humans

Nutrients

Volumn 10, Issue 5, 2018, Pages

  Crézé, Camille ^a   Candal, Laura ^a   Cros, Jérémy ^a   Knebel, Jean François ^b,c   Seyssel, Kevin ^a   Stefanoni, Nathalie ^a   Schneiter, Philippe ^a   Murray, Micah M ^b,c,d,e   Tappy, Luc ^a,f   Toepel, Ulrike ^b,c  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c University of Lausanne   (Switzerland)

^d VANDERBILT UNIVERSITY   (United States)

^e JULES GONIN EYE HOSPITAL   (Switzerland)

^f Hopital Intercantonal de la Broye   (Switzerland)

Author keywords

Ad libitum buffet; Electroencephalography; Food intake; Non nutritive sweeteners; Sweet taste; Visual food cues

Indexed keywords

GHRELIN; GLUCOSE; INSULIN; NONNUTRITIVE SWEETENER; SUCROSE; SWEETENING AGENT; NUTRITIVE SWEETENER;

ARTICLE; BEHAVIOR ASSESSMENT; CALORIC INTAKE; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; EXECUTIVE FUNCTION; FOOD INTAKE; HUMAN; HUNGER; INSULA; INTEROCEPTION; LIFESTYLE; LIPID DIET; LOW FAT DIET; MALE; NORMAL HUMAN; NUTRITION; PHYSICAL ACTIVITY; RANDOMIZED CONTROLLED TRIAL; RECOGNITION; SATIETY; SUGAR-SWEETENED BEVERAGE; THIRST; VENTROLATERAL PREFRONTAL CORTEX; VISUAL STIMULATION; BEVERAGE; BLOOD; BODY COMPOSITION; BODY MASS; BODY WEIGHT GAIN; BRAIN; CROSSOVER PROCEDURE; DECISION MAKING; DIET; DOUBLE BLIND PROCEDURE; FOOD PREFERENCE; GLUCOSE BLOOD LEVEL; HEALTH BEHAVIOR; METABOLISM; PHYSIOLOGY; POSTPRANDIAL STATE; TASTE;

BEVERAGES; BLOOD GLUCOSE; BODY COMPOSITION; BODY MASS INDEX; BRAIN; CHOICE BEHAVIOR; CROSS-OVER STUDIES; DIET; DOUBLE-BLIND METHOD; ELECTROENCEPHALOGRAPHY; ENERGY INTAKE; FOOD PREFERENCES; GHRELIN; HEALTH BEHAVIOR; HUMANS; HUNGER; INSULIN; MALE; NON-NUTRITIVE SWEETENERS; NUTRITIVE SWEETENERS; POSTPRANDIAL PERIOD; SATIATION; TASTE; WEIGHT GAIN;

EID: 85047099885     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu10050615     Document Type: Article

References (60)

1. DiMeglio, D.P.; Mattes, R.D. Liquid versus solid carbohydrate: Effects on food intake and body weight. Int. J. Obes. Relat. Metab. Disord. 2000, 24, 794–800. [CrossRef] [PubMed]
2. Malik, V.S.; Popkin, B.M.; Bray, G.A.; Després, J.P.; Hu, F.B. Sugar-sweetened beverages, obesity, type 2 diabetes mellitus, and cardiovascular disease risk. Circulation 2010, 121, 1356–1364. [CrossRef] [PubMed]
3. Vartanian, L.R.; Schwartz, M.B.; Brownell, K.D. Effects of soft drink consumption on nutrition and health: A systematic review and meta-analysis. Am. J. Public Health 2007, 97, 667–675. [CrossRef] [PubMed]
4. Dhingra, R.; Sullivan, L.; Jacques, P.F.; Wang, T.J.; Fox, C.S.; Meigs, J.B.; D’Agostino, R.B.; Gaziano, J.M.; Vasan, R.S. Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community. Circulation 2007, 116, 480–488. [CrossRef] [PubMed]
5. Fowler, S.P.; Williams, K.; Resendez, R.G.; Hunt, K.J.; Hazuda, H.P.; Stern, M.P. Fueling the obesity epidemic? Artificially sweetened beverage use and long-term weight gain. Obesity 2008, 16, 1894–1900. [CrossRef] [PubMed]
6. Stellman, S.D.; Garfinkel, L. Patterns of artificial sweetener use and weight change in an american cancer society prospective study. Appetite 1988, 11 (Suppl. 1), 85–91. [CrossRef]
7. Seeley, W.W.; Menon, V.; Schatzberg, A.F.; Keller, J.; Glover, G.H.; Kenna, H.; Reiss, A.L.; Greicius, M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27, 2349–2356. [CrossRef] [PubMed]
8. Berthoud, H.R. Metabolic and hedonic drives in the neural control of appetite: Who is the boss? Curr. Opin. Neurobiol. 2011, 21, 888–896. [CrossRef] [PubMed]
9. Laffitte, A.; Neiers, F.; Briand, L. Functional roles of the sweet taste receptor in oral and extraoral tissues. Curr. Opin. Clin. Nutr. Metab. Care 2014, 17, 379–385. [CrossRef] [PubMed]
10. Peng, Y.; Gillis-Smith, S.; Jin, H.; Tränkner, D.; Ryba, N.J.; Zuker, C.S. Sweet and bitter taste in the brain of awake behaving animals. Nature 2015, 527, 512–515. [CrossRef] [PubMed]
11. Schloegl, H.; Percik, R.; Horstmann, A.; Villringer, A.; Stumvoll, M. Peptide hormones regulating appetite–focus on neuroimaging studies in humans. Diabetes Metab. Res. Rev. 2011, 27, 104–112. [CrossRef] [PubMed]
12. Burke, M.V.; Small, D.M. Physiological mechanisms by which non-nutritive sweeteners may impact body weight and metabolism. Physiol. Behav. 2015, 152, 381–388. [CrossRef] [PubMed]
13. Swithers, S.E. Artificial sweeteners produce the counterintuitive effect of inducing metabolic derangements. Trends Endocrinol. Metab. 2013, 24, 431–441. [CrossRef] [PubMed]
14. Davidson, T.L.; Martin, A.A.; Clark, K.; Swithers, S.E. Intake of high-intensity sweeteners alters the ability of sweet taste to signal caloric consequences: Implications for the learned control of energy and body weight regulation. Q. J. Exp. Psychol. 2011, 64, 1430–1441. [CrossRef] [PubMed]
15. Wang, Q.P.; Lin, Y.Q.; Zhang, L.; Wilson, Y.A.; Oyston, L.J.; Cotterell, J.; Qi, Y.; Khuong, T.M.; Bakhshi, N.; Planchenault, Y.; et al. Sucralose promotes food intake through npy and a neuronal fasting response. Cell Metab. 2016, 24, 75–90. [CrossRef] [PubMed]
16. Bruyère, O.; Ahmed, S.H.; Atlan, C.; Belegaud, J.; Bortolotti, M.; Canivenc-Lavier, M.C.; Charrière, S.; Girardet, J.P.; Houdart, S.; Kalonji, E.; et al. Review of the nutritional benefits and risks related to intense sweeteners. Arch. Public Health 2015, 73, 41. [CrossRef] [PubMed]
17. Bruyère, O.; Ahmed, S.H.; Atlan, C.; Belegaud, J.; Bortolotti, M.; Canivenc-Lavier, M.C.; Charrière, S.; Girardet, J.P.; Houdart, S.; Kalonji, E.; et al. Erratum to: Review of the nutritional benefits and risks related to intense sweeteners. Arch. Public Health 2015, 73, 49. [CrossRef] [PubMed]
18. Renwick, A.G.; Molinary, S.V. Sweet-taste receptors, low-energy sweeteners, glucose absorption and insulin release. Br. J. Nutr. 2010, 104, 1415–1420. [CrossRef] [PubMed]
19. Shankar, P.; Ahuja, S.; Sriram, K. Non-nutritive sweeteners: Review and update. Nutrition 2013, 29, 1293–1299. [CrossRef] [PubMed]
20. Frank, G.K.; Oberndorfer, T.A.; Simmons, A.N.; Paulus, M.P.; Fudge, J.L.; Yang, T.T.; Kaye, W.H. Sucrose activates human taste pathways differently from artificial sweetener. Neuroimage 2008, 39, 1559–1569. [CrossRef] [PubMed]
21. Kilpatrick, L.A.; Coveleskie, K.; Connolly, L.; Labus, J.S.; Ebrat, B.; Stains, J.; Jiang, Z.; Suyenobu, B.Y.; Raybould, H.E.; Tillisch, K.; et al. Influence of sucrose ingestion on brainstem and hypothalamic intrinsic oscillations in lean and obese women. Gastroenterology 2014, 146, 1212–1221. [CrossRef] [PubMed]
22. Ginieis, R.; Franz, E.A.; Oey, I.; Peng, M. The “Sweet” Effect: Comparative assessments of dietary sugars on cognitive performance. Physiol. Behav. 2018, 184, 242–247. [CrossRef] [PubMed]
23. Dagher, A. Functional brain imaging of appetite. Trends Endocrinol. Metab. 2012, 23, 250–260. [CrossRef] [PubMed]
24. Van der Laan, L.N.; de Ridder, D.T.; Viergever, M.A.; Smeets, P.A. The first taste is always with the eyes: A meta-analysis on the neural correlates of processing visual food cues. Neuroimage 2011, 55, 296–303. [CrossRef] [PubMed]
25. Crézé, C.; Notter-Bielser, M.L.; Knebel, J.F.; Campos, V.; Tappy, L.; Murray, M.; Toepel, U. The impact of replacing sugar- by artificially-sweetened beverages on brain and behavioral responses to food viewing—An exploratory study. Appetite 2018, 123, 160–168. [CrossRef] [PubMed]
26. Oldfield, R.C. The assessment and analysis of handedness: The edinburgh inventory. Neuropsychologia 1971, 9, 97–113. [CrossRef]
27. Ordoñez, E.Y.; Rodil, R.; Quintana, J.B.; Cela, R. Determination of artificial sweeteners in beverages with green mobile phases and high temperature liquid chromatography-tandem mass spectrometry. Food Chem. 2015, 169, 162–168. [CrossRef] [PubMed]
28. Lietti, C.V.; Murray, M.M.; Hudry, J.; le Coutre, J.; Toepel, U. The role of energetic value in dynamic brain response adaptation during repeated food image viewing. Appetite 2012, 58, 11–18. [CrossRef] [PubMed]
29. Toepel, U.; Knebel, J.F.; Hudry, J.; le Coutre, J.; Murray, M.M. The brain tracks the energetic value in food images. Neuroimage 2009, 44, 967–974. [CrossRef] [PubMed]
30. Toepel, U.; Ohla, K.; Hudry, J.; le Coutre, J.; Murray, M.M. Verbal labels selectively bias brain responses to high-energy foods. Neuroimage 2014, 87, 154–163. [CrossRef] [PubMed]
31. Knebel, J.F.; Toepel, U.; Hudry, J.; le Coutre, J.; Murray, M.M. Generating controlled image sets in cognitive neuroscience research. Brain Topogr. 2008, 20, 284–289. [CrossRef] [PubMed]
32. Perrin, F.; Pernier, J.; Bertrand, O.; Giard, M.H.; Echallier, J.F. Mapping of scalp potentials by surface spline interpolation. Electroencephalogr. Clin. Neurophysiol. 1987, 66, 75–81. [CrossRef]
33. Murray, M.M.; Brunet, D.; Michel, C.M. Topographic erp analyses: A step-by-step tutorial review. Brain Topogr. 2008, 20, 249–264. [CrossRef] [PubMed]
34. Lehmann, D.; Skrandies, W. Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr. Clin. Neurophysiol. 1980, 48, 609–621. [CrossRef]
35. Toepel, U.; Bielser, M.L.; Forde, C.; Martin, N.; Voirin, A.; le Coutre, J.; Murray, M.M.; Hudry, J. Brain dynamics of meal size selection in humans. Neuroimage 2015, 113, 133–142. [CrossRef] [PubMed]
36. Michel, C.M.; Murray, M.M.; Lantz, G.; Gonzalez, S.; Spinelli, L.; Grave de Peralta, R. Eeg source imaging. Clin. Neurophysiol. 2004, 115, 2195–2222. [CrossRef] [PubMed]
37. Tataranni, P.A.; Gautier, J.F.; Chen, K.; Uecker, A.; Bandy, D.; Salbe, A.D.; Pratley, R.E.; Lawson, M.; Reiman, E.M.; Ravussin, E. Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proc. Natl. Acad. Sci. USA 1999, 96, 4569–4574. [CrossRef] [PubMed]
38. Jastreboff, A.M.; Sinha, R.; Arora, J.; Giannini, C.; Kubat, J.; Malik, S.; Van Name, M.A.; Santoro, N.; Savoye, M.; Duran, E.J.; et al. Altered brain response to drinking glucose and fructose in obese adolescents. Diabetes 2016, 65, 1929–1939. [CrossRef] [PubMed]
39. Weygandt, M.; Mai, K.; Dommes, E.; Leupelt, V.; Hackmack, K.; Kahnt, T.; Rothemund, Y.; Spranger, J.; Haynes, J.D. The role of neural impulse control mechanisms for dietary success in obesity. Neuroimage 2013, 83, 669–678. [CrossRef] [PubMed]
40. Lavagnino, L.; Arnone, D.; Cao, B.; Soares, J.C.; Selvaraj, S. Inhibitory control in obesity and binge eating disorder: A systematic review and meta-analysis of neurocognitive and neuroimaging studies. Neurosci. Biobehav. Rev. 2016, 68, 714–726. [CrossRef] [PubMed]
41. Camus, M.; Halelamien, N.; Plassmann, H.; Shimojo, S.; O’Doherty, J.; Camerer, C.; Rangel, A. Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex decreases valuations during food choices. Eur. J. Neurosci. 2009, 30, 1980–1988. [CrossRef] [PubMed]
42. Harris, A.; Hare, T.; Rangel, A. Temporally dissociable mechanisms of self-control: Early attentional filtering versus late value modulation. J. Neurosci. 2013, 33, 18917–18931. [CrossRef] [PubMed]
43. Critchley, H.D.; Wiens, S.; Rotshtein, P.; Ohman, A.; Dolan, R.J. Neural systems supporting interoceptive awareness. Nat. Neurosci. 2004, 7, 189–195. [CrossRef] [PubMed]
44. Menon, V.; Uddin, L.Q. Saliency, switching, attention and control: A network model of insula function. Brain Struct. Funct. 2010, 214, 655–667. [CrossRef] [PubMed]
45. Batterham, R.L.; ffytche, D.H.; Rosenthal, J.M.; Zelaya, F.O.; Barker, G.J.; Withers, D.J.; Williams, S.C. Pyy modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature 2007, 450, 106–109. [CrossRef] [PubMed]
46. Chambers, E.S.; Bridge, M.W.; Jones, D.A. Carbohydrate sensing in the human mouth: Effects on exercise performance and brain activity. J. Physiol. 2009, 587, 1779–1794. [CrossRef] [PubMed]
47. Connolly, L.; Coveleskie, K.; Kilpatrick, L.A.; Labus, J.S.; Ebrat, B.; Stains, J.; Jiang, Z.; Tillisch, K.; Raybould, H.E.; Mayer, E.A. Differences in brain responses between lean and obese women to a sweetened drink. Neurogastroenterol. Motil. 2013, 25, 579-e460. [CrossRef] [PubMed]
48. Small, D.M. Flavor is in the brain. Physiol. Behav. 2012, 107, 540–552. [CrossRef] [PubMed]
49. Hopfinger, J.B.; Buonocore, M.H.; Mangun, G.R. The neural mechanisms of top-down attentional control. Nat. Neurosci. 2000, 3, 284–291. [CrossRef] [PubMed]
50. Killgore, W.D.; Young, A.D.; Femia, L.A.; Bogorodzki, P.; Rogowska, J.; Yurgelun-Todd, D.A. Cortical and limbic activation during viewing of high- versus low-calorie foods. Neuroimage 2003, 19, 1381–1394. [CrossRef]
51. Führer, D.; Zysset, S.; Stumvoll, M. Brain activity in hunger and satiety: An exploratory visually stimulated fmri study. Obesity 2008, 16, 945–950. [CrossRef] [PubMed]
52. Alonso-Alonso, M.; Pascual-Leone, A. The right brain hypothesis for obesity. JAMA 2007, 297, 1819–1822. [CrossRef] [PubMed]
53. Smeets, P.A.; Weijzen, P.; de Graaf, C.; Viergever, M.A. Consumption of caloric and non-caloric versions of a soft drink differentially affects brain activation during tasting. Neuroimage 2011, 54, 1367–1374. [CrossRef] [PubMed]
54. Berthoud, H.R. The neurobiology of food intake in an obesogenic environment. Proc. Nutr. Soc. 2012, 71, 478–487. [CrossRef] [PubMed]
55. Berridge, K.C. ‘liking’ and ‘wanting’ food rewards: Brain substrates and roles in eating disorders. Physiol. Behav. 2009, 97, 537–550. [CrossRef] [PubMed]
56. Kringelbach, M.L. The human orbitofrontal cortex: Linking reward to hedonic experience. Nat. Rev. Neurosci. 2005, 6, 691–702. [CrossRef] [PubMed]
57. Mitchell, D.G. The nexus between decision making and emotion regulation: A review of convergent neurocognitive substrates. Behav. Brain Res. 2011, 217, 215–231. [CrossRef] [PubMed]
58. Green, E.; Murphy, C. Altered processing of sweet taste in the brain of diet soda drinkers. Physiol. Behav. 2012, 107, 560–567. [CrossRef] [PubMed]
59. Rudenga, K.J.; Small, D.M. Amygdala response to sucrose consumption is inversely related to artificial sweetener use. Appetite 2012, 58, 504–507. [CrossRef] [PubMed]
60. Verhagen, J.V. The neurocognitive bases of human multimodal food perception: Consciousness. Brain Res. Rev. 2007, 53, 271–286. [CrossRef] [PubMed]