Beverage consumption, appetite, and energy intake: what did you expect?
Bridget A. Cassady, Robert V. Considine, and Richard D. Mattes. Am J Clin Nutr. 2012;95(3):587-93.
BACKGROUND:
Beverage consumption is implicated in the overweight/obesity epidemic through the weaker energy compensation response it elicits compared with solid food forms. However, plausible mechanisms are not documented.
OBJECTIVE:
This study assessed the cognitive and sensory contributions of differential postingestive responses to energy- and macronutrient-matched liquid (in beverage form) and solid food forms and identifies physiologic processes that may account for them.
DESIGN:
Fifty-two healthy adults [mean ± SD age: 24.7 ± 5.5 y; BMI (in kg/m(2)): 26.3 ± 6.3] completed this randomized, 4-arm crossover study. Participants consumed oral liquid and solid preloads that they perceived, through cognitive manipulation, to be liquid or solid in their stomach (ie, oral liquid/perceived gastric liquid, oral liquid/perceived gastric solid, oral solid/perceived gastric liquid, or oral solid/perceived gastric solid). However, all preloads were designed to present a liquid gastric challenge. Appetite, gastric-emptying and orocecal transit times, and selected endocrine responses were monitored for the following 4 h; total energy intake was also recorded.
RESULTS:
Oral-liquid and perceived gastric-liquid preloads elicited greater postprandial hunger and lower fullness sensations, more rapid gastric-emptying and orocecal transit times, attenuated insulin and glucagon-like peptide 1 release, and lower ghrelin suppression than did responses after oral-solid and perceived gastric-solid treatments (all P < 0.05). Faster gastric-emptying times were significantly associated with greater energy intake after consumption of perceived gastric-liquid preloads (P < 0.05). Energy intake was greater on days when perceived gastric-liquid preloads were consumed than when perceived gastric solids were consumed (2311 ± 95 compared with 1897 ± 72 kcal, P = 0.007).
CONCLUSIONS:
These data document sensory and cognitive effects of food form on ingestive behavior and identify physical and endocrine variables that may account for the low satiety value of beverages. They are consistent with findings that clear, energy-yielding beverages pose a particular risk for positive energy balance. This study was registered at clinicaltrials.gov as NCT01070199.
Opening Comments
Today’s topic is one of much intrigue and debate, particularly because of liquid calories being implicated in today’s obesity epidemic. It is no secret that we drink more soft drinks today than we did 50 years ago [1], but simply saying that soft drinks cause obesity is flat out foolish, for reasons I will make explicit in a little bit. What merely started as a short article review quickly turned into more of an in-depth research review, but I promise it is well worth the read. So without much further ado, let’s delve in!
…But right after a quick announcement
Sorry, but before I get into today’s topic, I need to make myself perfectly clear from the very start. Because this topic somewhat overlaps with the “Great High-fructose Corn Syrup (HFCS) Debate,” the distinction between the two topics must be made now before I have people misquoting me later on. Got it? Good.
The Distinction
I believe I made myself pretty clear two months ago when I argued that HFCS is not the cause obesity. Obesity is a multi-factorial condition, meaning that it has many causes, and therefore picking one factor out of a whole host of other collinear factors (such as reduced physical activity, high-calorie foods, and greater caloric intake overall) is foolish and forms the basis of a very weak argument. HOWEVER, over the years there has been a lot of research done on the non-satiating (not filling) effects of liquid calories (i.e. soda, juices, sports drinks and the like (which commonly use HFCS as a sweetener)) and how they make us consume more food than solid foods do. The idea that the energy from caloric beverages, as opposed to solid foods, is poorly compensated for is not a new concept [2-6]. In fact, the topic has been studied as early as the late 1970’s and continues to this day.
A substantial amount of the literature suggests that liquid calories are not efficiently compensated for by physiologic responses in the brain and therefore do not cause us to reduce food intake as much as a solid foods do [7]. This is important because it draws the distinction between beverages and solid foods and their subsequent effects on appetite and potential weight gain. One of the more interesting studies (given the upcoming Easter season), conducted by DiMeglio and Mattes in 2000 [8], observed the effects of 450kcals of either soda or jelly beans on subsequent food intake over the course of the day. It was shown that people who consumed the jelly beans slightly decreased their food intake over the course of the day while the soda group not only ate as much as they usually did but actually ate slightly more. This study implies that, not only are liquid calories inferior to solid calories in terms of compensating food intake, but also that it doesn’t matter which sweetener is used but rather the vehicle in which that sweetener is added to (i.e. solid or liquid). Re-read that sentence if you have to. Therefore, HFCS (or any sweetener for that matter) in a beverage (like soda) would not have the same effect on appetite and food intake as HFCS in a solid product would. That’s, at least, what the research is looking like thus far, although I do have some reservations which will be made evident later on. But, before I get ahead of myself, let’s get back to the paper at hand.
As I was saying, it looks like beverages seem to be inferior to solid foods when it comes to appetite and food intake, however, a specific mechanism for why we can’t compensate for liquid calories as well as we do for solid calories is the question which today’s article tries to answer. Also, an extremely interesting (and historical) paper, written by Georgy A. Bray and Barry M. Popkin, on why we can’t compensate for liquid calories can be found here for those who are interested. The authors essentially claim that our ancestors did not drink anything other than water and breast-milk, the latter which is only important for babies, for most their human evolution and therefore did not evolve a physiologic mechanism to compensate for liquid calories. It’s a very easy read if you’re so inclined. However, let’s get back to today’s article and see why liquid calories might not be compensated for as well as solid calories are.
The Study
Today’s article essentially looks at the same exact outcomes that previous studies have looked at (i.e. satiety and subsequent food intake); however this study throws a whole other factor into the mix, which is the human mind. Here, the researchers wanted to see how perceptions of beverages and solid foods would (if at all) influence metabolism, satiety, and subsequent food intake. This is extremely interesting because it asserts that we can essentially control how full we are and how well we digest liquids based solely off of how we perceive a food’s effect in our body regardless of its physical state. I know crazy, right? This concept actually falls perfectly in line with the thinking that people eat less at dinner after they have soup. In fact, it has been consistently observed in acute studies that people consume fewer calories from a meal after the ingestion of soup [9-14]. Moreover, in a recent study done with children aged 3-5 years, similar effects were shown when the children received a small portion of tomato soup right before lunch [15]. However, the actual mechanism for why soups – and not other liquids – induce satiety has never been accurately identified, although today’s study may provide some insight.
Participants (n = 52) were exposed to 4 separate experimental conditions with a wash-out period between each protocol. The 4 conditions were; liquid-liquid, liquid-solid, solid-liquid, and solid-solid. The liquid-liquid (L-L) condition meant that subjects were given a caloric beverage and were told it would remain liquid in their stomach. The liquid-solid (L-S) condition was the same exact beverage however they were told that the beverage would turn to a solid in their stomach (when in fact it was the same beverage as the L-L). The solid-liquid (S-L) treatment was a gelatin cube in which participants were told would turn to liquid in their stomachs, and the solid-solid (S-S) treatment was the same exact cube aside from being told it would remain a solid in participant’s stomachs.
After ingestion of the beverages or cubes subjects were told to rate their satiety every half hour for a total of 4 hours. Also, breath tests and blood samples were taken to measure the rate of digestion of the beverage or cube and the concentrations of certain hormones associated with hunger and satiety. At the end of 4 hours they were each given a plate of macaroni and cheese and were told to eat until they felt full.
The Results
Subjects who were told that the liquid solution would remain a liquid in their stomach (L-L) digested it faster than those who thought the beverage would turn into a solid in their stomach (L-S). This happened even though it was, again, the exact same liquid beverage. The only difference was what the researchers told them would happen. Furthermore, receiving the L-L beverage made people rank their satiety as being much lower than when given the L-S beverage, also causing them to eat more calories (~130kcals more) when given a meal 4 hours later.
Similarly, those who believed an isocaloric gelatin (solid) cube would turn into a liquid in their stomach (S-L) digested the cube much faster than those who thought the same cube would remain solid in their stomach (S-S). Just as before, when subjects received a food they though would be liquid in their stomachs, they ranked their satiety as being much lower than when given a food they thought would remain solid in their stomachs. Also, the S-S cube resulted in the least amount of calories eaten from the plate of macaroni across all treatments.
Overall, the L-L and L-S beverages were digested faster than the S-L and S-S cubes (as seen by breath tests), adding to the literature that transit time of a liquid through the GI tract may also play a role in perceived satiety (faster transit = lower satiety) [16-18]. However, to quote the authors;
“The findings indicate that the mere expectation that a food will be in one form or another in the [GI] tract produces behavioral and physiologic responses likely to contribute to lower satiety effects and weaker dietary compensation after beverage ingestion.”
Simply put, just by thinking a food or beverage will act a certain way in your stomach actually dictates how you will digest that food and how full you will actually feel regardless of the physical state that food or beverage is actually in. This lends credence to research involving soup. Soups are predominantly liquids (yes there are some vegetables in some of them) yet most people perceive them to be foods (solids). Having soup before a meal could reduce hunger and improve satiety based solely on our perceptions of that soup – i.e. that it will make us feel full because we think it’s a solid-food rather than a liquid one. However, whether or not this is relevant towards the obesity epidemic is something I will talk about in a little bit.
To go back and further expand upon the blood samples/measurements, I should also note that ghrelin, a hormone related directly to hunger, was seen to be higher after the L-L and L-S beverages compared to the S-L and S-S cubes, correlating strongly to the higher perceived hunger seen in the participants after they consumed the liquid solutions. Again, just to reiterate, there were no differences between the beverages besides what the researchers told the participants. The same goes for the solid cubes, which, I might add, also turned to liquid in the stomach and therefore weren’t much different from the liquid solutions aside from the participants having to masticate.
Still, even though the solutions and cubes were essentially all identical people’s perceptions dictated their physiologic responses which made them feel more or less full. This led participants to eat more or less food 4 hours later when given a meal. Pretty profound results, if I say so myself.
My Thoughts
One thing to consider – and this is the one caveat I will stress when looking at satiety papers dealing with liquid calories – is the time delay seen between the administration of the liquids/cubes and the subsequent meal which was given 4 hours later. Most studies which show similar results use similar protocols when administering a meal [19-21]. However, given that the pre-loads were not administered in close proximity to the meal (like the soup studies I mentioned earlier) we don’t know if the results would have been different had the meal been given sooner. A lot of other studies show that liquid calories in fact do cause people to reduce caloric intake, although these studies used fairly large pre-loads (>600mL) and gave the meal close to immediately afterwards (0-30 minutes) [22]. Due to the differences used in the time between pre-load and the meal, it makes it hard to argue one way or the other without taking into context the way in which the liquid is consumed. To quote the authors of a well-written review on liquid calories and failed satiety [22];
“The controversy regarding liquid foods and the supposed failure of satiety may be resolved if we consider the time elapsed between the [beverage] and the [meal]… Whether energy is provided in liquid or solid form may be less important than the timing of intake and the context in which it is consumed.”
Application/Relevance with Regards to the Obesity Epidemic
Although this study is extremely interesting and truly shows the power of the mind over physiology, I do not see how the results relate much to the obesity epidemic at hand. No one in their right mind thinks soda or juice would turn into a solid in their stomach. Therefore, it’s pretty safe to say that people’s perceptions of commonly consumed beverages (unlike soups) won’t change anytime soon. Consequently, the results seen here are purely academic and are nonetheless irrelevant to normal human consumption of beverages, which right now are sodas, juices, sports drinks and the like which potentially cause us to eat more. That is unless companies start marketing a liquid-solid soda or something similar to those Shot-Blocs made by Clif® that will stay as a solid in the stomach. Maybe then people would start reducing their calories throughout the day, however, I doubt that will happen. So, in the end, the results are cool but not extremely relevant given common perceptions of sodas and juices which are the main supposed culprits in today’s epidemic.
Summary
So, are liquid calories to blame for the obesity epidemic? Well, the preponderance of studies, including this one, which similarly deliver a meal 2-4 hours after the pre-load, seem to suggest that liquid calories may be involved. Due to the fact that sodas and sugar-sweetened beverages (SSB) aren’t soups, nor will they ever be perceived as foods (solids in the stomach), it seems that they may be a contributor to the obesity epidemic, although they are by no means THE CAUSE. I cannot stress this enough. Obesity is a multi-faceted problem and no one factor will ever be seen as the root-cause. Certain factors may contribute while others may seem to help, however, in the end it comes down to what we put in and what we put out. My personal views, habits, and opinions on sodas are as follows:
1. I don’t particularly like soda, but I defend the right to sell/drink it. Just don’t be a lazy bum and you can enjoy the occasional sugar-sweetened beverage (SSB) every now and again. Even if soda did cause you to increase caloric intake (aside from it being a source of calories itself), if your energy expenditure (exercise) is still more than what you put in, soda will never cause you to gain weight.
2. I myself do not drink SSBs (Hell, I don’t even put sugar in my coffee). I was not raised in a household where we drank soda or juice and I believe SSBs displace calories I could easily get from better food sources.
3. Lastly, if you absolutely MUST have soda, switch to diet. Even if you do eat as much as you would have, you still get the soda without the added calories and can maintain caloric balance.
I will end with noting that I did not talk much about alcohol, an extremely popular beverage among the US population and one which does offer calories. Being a college student myself I would be lying if I said undergraduates don’t consume alcohol. That being said, it seems that alcohol, too, does not offer a compensatory response for energy intake, leading to greater consumption even when alcohol is given immediately (30 minutes or less) before the meal [23-25]. Although it would make sense that drinkers would be heavier than non-drinkers due to the lack of caloric compensation, this appears not to be the case [26, 27]. Possible reasons for why drinkers are not heavier than non-drinkers could be due to the fact that people who have higher alcohol intakes might also have higher levels of physical activity on those days (see statement 1 above) [28].
So no matter what you choose to drink, remember that SSBs and the like ARE calories and you might not get the same satiating power you would get from a solid food, causing you to consume more later on. On the whole, anything you could derive from a soda (which is essentially just sugar) you could equally (if not beneficially) obtain from a better food source. I’d leave it at that.
References
1. Economic Research Service, USDA. Food availability data. Updated February 1, 2011.
2. Pliner PL. Effect of liquid versus solid preloads on eating behavior of obese and normal persons. Physiol Behav 1973;11:285-290.
3. Malagelada JR, Go VLW, Summerskill WHJ. Differential gastric, pancreatic, and biliary responses to solid-liquid or homogenous meals. Dig Dis Sci 1979;24:101-110.
4. Kissileff HR, Klingsberg G, Van Itallie T. Universal eating monitor for continuous recording of solid or liquid consumption in man. Am J Physiol 1980;238:R14-R22.
5. Jordan HA, Levitz LS, Utgoff KL, Lee HL. Role of food characteristics in behavioral change and weight loss. JADA 1981;79:24-29.
6. Mustad VA, Jonnalagadda SS, Smutko SA, Pelkman CL, Rolls BJ, Behr SR, Pearson TA, Kris-Etherton PM. Comparative lipid and lipoprotein responses to solid-food diets and defined liquid-formula diets. Am J Clin Nutr 1999;70:839-846.
7. Mattes RD. Fluid energy – where’s the problem? JADA 2006;106(12):1956-61.
8. DiMeglio DP, Mattes RD. Liquid versus solid carbohydrate: effects on food intake and body weight. Int J Obes Relat Metab Disord 2000;24:795-800.
9. Rolls BJ, Federoff IC, Guthrie JF, Laster LJ. Foods with different satiating effects in humans. Appetite 1990;15:115-126.
10. Jordan HA, Levitz LS, Utgoff KL, Lee HL. Role of food characteristics in behavioral change in weight loss. JADA 1981;79:24-29.
11. Kissileff HR. Effects of physical state (liquid-solid) of foods on food intake: Procedural and substantive contributions. Am J Clin Nutr 1985;42:956-965.
12. Rolls BJ, Bells EA, Thorwart ML. Water incorporated into food but not served with a food decreases energy intake in lean women. Am J Clin Nutr 1999;70:448-455.
13. Mattes RD. Soup and satiety. Physiol Behav 2005;83:739-747.
14. Flood JE, Rolls BJ. Soup preloads in a variety of forms reduce meal energy intake. Appetite 2007;48:626-634.
15. Spill MK, Birch LL, Roe LS, Rolls BJ. Serving large portions of vegetable soup at the start of a meal affected children’s energy and vegetable intake. Appetite 2011;57(1):213-9.
16. Jian R, Ducrot F, Najean Y, Cortot A, Modigliani R. Effect of alcohol on gastric empting of an ordinary meal in man. Gut 1983;24:A363.
17. Marciani L, Gowland PA, Spiller RC, Manoj P, Moore RJ, Young P, Fillery-Travis AJ. Effect of meal viscosity and nutrients on satiety, intragastric dilution, and emptying assessed by MRI. Am J Physiol Gastrointest Liver Physiol 2001:280(6):G1227-33.
18. Marciani L, Gowland PA, Spiller RC, Manoj P, Moore RJ, Young P, Al-Sahab S, Bush D, Wright J, Fillery-Travis AJ. Gastric response to increased meal viscosity assessed by echo-planar magnetic resonance imaging in humans. J Nutr 2000;130(1):122-7.
19. Mattes RD. Dietary compensation by humans for supplemental energy provided as ethanol or carbohydrates in fluids. Physiol Behav 1996;59:179-187.
20. Drewnowski A, Massien C, Louis-Sylvestre J, Fricker J, Chapelot D, Apfelbaum M. The effects of aspartame versus sucralose on motivational ratings, taste preferences ad energy intakes in obese and lean women. Int J Obes Relat Metab Disord 1994;18:570-578.
21. De Graaf C, Hulshof T, Weststrate JA, Jas P. Short-term effects of different amounts of protein, fats, and carbohydrates on satiety. Am J Clin Nutr 1992;55:33-38.
22. Almiron-Roig E, Chen Y, Drewnowski A. Liquid calories and the failure of satiety: how good is the evidence? Obesity 2003;4:201-212.
23. Westerterp-Plantenga MS, Verwegen CRT. The appetizing effect of an aperitif in overweight and normal-weight humans. Am J Clin Nutr 1999;69:205-212.
24. Heatherington MM, Cameron F, Wallis DJ, Pirie LM. Stimulation of appetite by alcohol. Physiol Behav 2001;74:283-289.
25. Poppitt SD, Eckhardt JW, McGonagle J, Murgatroyd PR, Prentice AM. Short-term effects of alcohol consumption on appetite and energy intake. Physiol Behav 1996;60:1063-1070.
26. Alcohol consumption, nutrient intake and relative body weight among US adults. Am J Clin Nutr 1985;42(2):289-295.
27. Colditz GA, Giovannucci E, Rimm EB, Stampfer MJ, Rosner B, Speizer FB, Gordis E, Willett WC. Alcohol intake in relation to diet and obesity in women and men. Am J Clin Nutr 1991;54(1):49-55.
28. Westerterp KR, Meijer EP, Goris AH, Kester AD. Alcohol energy intake and habitual physical activity in older adults. Br J Nutr 2004;91(1):149-52.
Calories in Context 
You have to wonder what the role of our evolution to love glucose has done to our ability to get satiety from sugary foods. If you think about it, we love sugar and will generally keep eating it obsessively. The contents of a soda pure sugar with water, flavor, and carbonation. We are hard wired (just do a good search for “hedonic reward glucose”) to want more sugar because it would not normally be available to us in olden times so we want as much as we can get. Some will say that we don’t eat endless amounts of cake and that is just as sugary, but cake has large amounts of fat and that makes us full. The sensitivity to fat and the satiety from fat is why it is recommended that you 1 oz of cream cheese with that bagel at breakfast because it will keep you full longer and let you make it to lunch without snacking. Soda has carbonation which makes your stomach expand so it is probably not a question of enlarging the stomach (engaging stretch mechanioreceptors). I would presume that we love sugar and our bodies don’t have a good system to say enough is enough, lay off the sugar.
You should definitely read the paper by Popkin that I linked in my article. It’s a quick/interesting read and offers a reasonable hypothesis for why we cannot compensate for liquid calories. The research seems to support this theory although the mechanism is still unknown.
As far as your comment about us being “hard-wired” to obsessively eat sugar, I’m not 100% this is the case. There is a good study (Nummenmaa et al. 2012) which shows that obesity is the potential modulator of the reward circuit in the brain, meaning that those who are obese have much different limbic responses to glucose than do normal weight counterparts. This could potentially explain why obese people continue to overeat despite being morbidly obese. Obviously not all people obsessively eat sugar, nor does everyone respond to sugar in the same way, as evidenced by Nummenmaa et al. 2012. However, the question stills remains: were the obese participants predisposed to becoming obese because they respond to glucose differently? It’s the chicken or the egg question. To me the problem doesn’t lie with sugar per se. Rather, it is the vehicle for which sugar is consumed. You somewhat alluded to this with your statement about cake. SSBs do not contain fiber, fat, protein, etc. which make them much more different than every other food source we consume, even candy which requires some degree of mastication.
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