The food reward hypothesis of obesity states that the reward and palatability value of food influence body fatness, and excess reward/palatability can promote body fat accumulation. If we want to test the hypothesis, the most direct way is to find experiments in which 1) the nutritional qualities of the experimental diet groups are kept the same or at least very similar, 2) some aspect of diet reward/palatability differs, and 3) changes in body fat/weight are measured (for example, 2, 3, 4, 5, 6, 7, 8, 9). In these experiments the hypothesis has both arms and one leg tied behind its back, because the most potent reward factors (energy density, sugar, fat) have nutritional value and therefore experiments that modify these cannot be tightly controlled for nutritional differences. Yet even with this severe disadvantage, the hypothesis is consistently supported by the scientific evidence. Taubes repeatedly stated in his series that controlled studies like these have not been conducted, apparently basing this belief on a 22-year-old review paper by Dr. Israel Ramirez and colleagues that does not contain the word 'reward' (10).
Another way to test the hypothesis is to see if people with higher food reward sensitivity (due to genetics or other factors) tend to gain more fat over time (for example, 11, 12, 13, 14, 15, 16). In addition, studies that have examined the effect of palatability/reward on food intake in a controlled manner are relevant (17, 18, 19, 20, 21, 22), as are studies that have identified some of the mechanisms by which these effects occur (reviewed in 23). Even if not all of the studies are perfect, at some point, one has to acknowledge that there are a lot of mutually buttressing lines of evidence here. It is notable that virtually none of these studies appeared in Taubes's posts, and he appeared largely unaware of them.
I'd like to briefly discuss three studies Taubes brought up, because I think they encapsulate the nature of this debate nicely. The first study is the only sugar consumption study Taubes cited in which 1) palatability was somewhat controlled for, and 2) body fat changes were actually measured (although none of the sugar studies cited were designed to investigate the effects of reward/palatability on body fat accumulation). Taubes suggests in his series that a more compelling hypothesis is that dietary fructose promotes fat gain, and I suppose the relevance is that if this idea is true, it weakens the food reward hypothesis (the reasoning here eludes me). Dr. Peter Havel’s group fed volunteers fructose or glucose-sweetened beverages as 25% of their total calorie intake, for 10 weeks (24). If fructose has some special ability to increase body fatness that glucose does not have, then the fructose group should have gained more fat. Here’s what they observed:
Body fat mass increased by about 3% in both groups (slightly but not significantly higher in the glucose group), despite the fact that fasting insulin increased by 10.2% in the fructose group and only 2.9% in the glucose group. It is puzzling that this piece of information did not appear in Taubes's discussion of the paper, when it is the only element of the study that is relevant to the question at hand. The fructose group gained more fat in the abdominal (belly) region, and less in other places, and experienced negative metabolic changes, which is why I discussed this paper in 2009 (25). But if we’re trying to figure out what causes obesity, aren’t we talking about body fat accumulation? This study shows that sweetened beverages, regardless of fructose content, and regardless of effects on circulating insulin, cause body fat accumulation in humans when added to a typical diet. I'm not sure how that argues against the food reward hypothesis of obesity, but it certainly poses a challenge for the fructose and insulin hypotheses of obesity.
All reviewed studies have shown increased intake as palatability increased...
Studies also measuring the effect of palatability on energy intake (the ‘within-meal’ effect) show increased intake as palatability increases, no matter what the effect of palatability on the subjective appetite sensations is.
The third study I'd like to discuss is the weight loss study I introduced in previous posts, in which obese people (but not lean people) dramatically reduced their calorie intake and lost body fat when restricted to a bland and repetitive liquid diet consumed through a straw (34). Taubes objected that the liquid diet was not low in palatability/reward value because it was sweet, which is the same objection he brought up after my talk at the Ancestral Health Symposium. This truly strains the imagination. Let's do a thought experiment here. What would you rather eat for two weeks straight, this:
Nestle Nutrament, the modern version of the formula that was used in the study. Ingredients: Skim milk, sugar, corn syrup, canola oil, high oleic sunflower oil, calcium caseinate, soy protein isolate, corn oil, sodium caseinate, artificial flavour, magnesium phosphate, magnesium chloride, carrageenan, soy lecithin, sodium ascorbate, ferrous sulfate, zinc sulfate, vitamin E acetate, niacinamide, calcium pantothenate, cupric sulfate, manganese sulfate, vitamin A palmitate, vitamin B6 hydrochloride, thiamine hydrochloride, riboflavin, chromium chloride, folic acid, vitamin D3, biotin, sodium molybdate, sodium selenite, vitamin K1, vitamin B12.
Or a typical varied diet? If you ate nothing but Nutrament, described by the investigators at the time as a "bland liquid formula", day in and day out, would you find it delicious? Would you wake up excited to drink it every morning? Would you choose a meal of this liquid over a steak, baked potato and salad? How about scrambled eggs, hash browns and coffee? Amazingly, Taubes argues that this would not have been a low-reward/palatability situation (35).
Furthermore, he does not seem to be bothered by the fact that two (out of two where weight changes were reported) obese patients rapidly lost body fat on a diet that was 50 percent highly refined carbohydrate, including a high proportion of sugar, even though they were asked to drink the liquid to fullness. I thought refined carbohydrate and sugar were supposed to drive insulin, hunger and body fat accumulation? Taubes attempted to reconcile this by suggesting that all five obese patients (out of five where calorie intake was described) were deliberately restricting calories to lose fat during the study (35b). If all five of these people had the desire and stoic determination to eat 400 calories a day for an extended period of time, why hadn't they already done so prior to the study? Not to mention the fact that the subjects reported not being hungry. According to Taubes, this was because their low calorie intake meant they weren't consuming much carbohydrate, therefore their insulin dropped, their fat was "unlocked" and they burned it instead of needing food (35b)! So all we have to do is go on a 400-calorie diet, our insulin will drop, and the pounds will melt off without any hunger? Eureka! I find these logical contortions highly entertaining.
This study demonstrates that in a low-palatability/reward context, refined carbohydrate and sugar can actually allow substantial fat loss, suggesting that they are not inherently fattening, but rather that their ability to cause fat accumulation depends on their palatability/reward value. This is probably a central reason why people who get most of their calories from white rice (e.g., large parts of Asia) are typically lean, not obese as one would expect if refined carbohydrate were inherently fattening.
I could keep going, but I think you get the point. In his critique, Taubes demonstrated neither a knowledge of the relevant literature, nor a willingness to accurately interpret the papers he did encounter. Therefore, I don't see any need to respond in a more comprehensive manner. However, I did compose something that I think will be more useful to the readership, which is a deconstruction of the core argument that Taubes uses to brush aside 60 years obesity research that would otherwise falsify many of his ideas (below). It is also the same argument he uses to attempt to discredit obesity researchers who hold ideas that are not consistent with his own (i.e., nearly all of them).
The evidence supporting the food reward hypothesis continues to speak for itself:
The Case for the Food Reward Hypothesis of Obesity, Part I
The Case for the Food Reward Hypothesis of Obesity, Part II
Food Palatability and Body Fatness: Clues from Alliesthesia
Food Reward, a Dominant Factor in Obesity, I, II, III, IV, V, VI, VII, VIII
Humans on a Cafeteria Diet
Losing Fat With Simple Food-- Two Reader Anecdotes
The evidence arguing against the carbohydrate-insulin hypothesis of obesity also continues to speak for itself:
The Carbohydrate Hypothesis of Obesity: a Critical Examination
Hyperinsulinemia: Cause or Effect of Obesity?
Does High Circulating Insulin Drive Body Fat Accumulation? Answers from Genetically Modified Mice
Fat Tissue Insulin Sensitivity and Obesity
Clarifications About Carbohydrate and Insulin
The "Energy Balance Paradigm" Argument: a Red Herring
Rather than compose a full rebuttal to Taubes's recent posts, I thought it would be more productive to discuss one of the core elements of his position, which has arguably been one of his greatest influences on the public. This is the "paradigm shift" he promotes, away from thinking about obesity as a problem of energy imbalance (energy in vs. out), and toward thinking about it as a "disorder of excess fat accumulation" where energy imbalance is the result rather than the cause of fat tissue expansion (36). He seems to believe that thinking about energy balance at all is a distraction, and framing obesity in those terms is enough to send a paper to the dustbin (37). He uses this argument to brush aside much of the last 60 years of obesity research, and the opinions of many seasoned researchers, arguing that they are largely irrelevant because they operate under the wrong paradigm (logical framework).
Maybe I'm a little slow, but only recently did I realize just how much of a red herring this argument is. It has generated a lot of confusion and ill will toward researchers over the years, and it's time to shine a light on it.
Calorimetry is the science of measuring energy release in the form of heat, often from living organisms. The first documented attempts to quantify energy expenditure in a living animal were likely performed by Dr. Antoine Lavoisier and colleagues in the 18th century, according to an excellent review paper on calorimetry by my friend Dr. Karl Kaiyala (38). Calorimetry tools improved greatly in the late 19th century, including calorimeters of sufficient size to measure human energy expenditure, and it has been a staple technique in a number of fields, including obesity research, since then. Calorimetry also permits the measurement of the energy content of foods, so it provides information about both the "in" and the "out" side of the equation.
The first law of thermodynamics states that energy cannot be created or destroyed, only shuttled between different forms (e.g., chemical energy and heat). In this context, what it means is that changes in the energy content of a human body depend strictly on the amount of energy entering it, minus the amount leaving it. This was empirically confirmed by a series of extraordinary experiments by Dr. Wilbur Atwater and colleagues in the late 1800s, a summary of which was published in 1899 and is freely accessible online (39). Since body fat is by far the main modifiable energy storage site in the human body (i.e., other organs don't have the ability to change their energy content very much), one would predict that the long-term balance between energy in and energy out would determine fat mass stores. This is indeed the case (40, 41, 42, 43).
When researchers discovered that fat mass depends tightly on energy balance in humans, they realized that they has discovered the cause of, and solution to, obesity. Obesity is caused by energy entering the body at a greater rate than it leaves, and fat loss occurs when this is reversed. This is simply a fact at this point, and it has been repeatedly confirmed (44, 45, 46, 47, 48). However, it is an incomplete explanation, because it doesn't tell us why the energy imbalance is present (therefore, it is the proximal, rather than the ultimate cause), and it does not necessarily imply that simply asking people to eat less and move more is a practical solution to obesity. This is where I agree with Taubes-- 1) the key thing to understand is what is causing the energy imbalance, and 2) the idea that "eat less, move more" is a practical fat loss strategy does not necessarily follow from the first law of thermodynamics. Taking in less energy and expending more does cause fat loss, but the problem is that it's difficult to maintain-- the body opposes changes in its fat stores. However, this is where the usefulness of his idea ends.
It has been made clear by countless studies that body fat stores can be manipulated by changing food intake and energy expenditure. For example, overfeeding reliably increases fat mass in humans and can produce substantial body fat accumulation, regardless of whether the excess calories come from carbohydrate or fat, and regardless of changes in circulating insulin (49, 50, 51, 52). Similarly, underfeeding reliably decreases fat mass by a predictable amount, also regardless of macronutrients and changes in circulating insulin (53, 54, 55). "Exceptions" to this rule only seem to occur in studies where food intake is not measured accurately.
To some extent, changes in fat mass are opposed by the body (under the direction of the brain), for example, energy expenditure decreases with fat loss and this is largely dependent on the reduction in circulating leptin that accompanies fat loss (56). Not everyone gains the same amount of fat mass when overfed, because certain people can ramp up energy expenditure to some degree, but this is fairly limited and the effect remains controversial. These adaptive changes in energy expenditure depend on the location of the body fat "setpoint" (or whatever you want to call it), as I have discussed in previous posts. However, all of this can be accounted for by changes in energy expenditure, and thus none of it violates the first law of thermodynamics.
The primary role of fat tissue is to buffer body energy stores, absorbing excess energy and storing it for when it is needed and keeping it away from the other tissues where it would do damage, and that is exactly what it does in response to changes in energy balance. Regardless of the hormonal milieu of the body (with the exception of a few rare and severe disorders), when energy balance (in vs. out) is experimentally altered, it is reflected tightly in fat mass stores.
To review the key points so far:
- Energy balance tightly determines changes in body fat stores
- This does not necessarily imply that "eat less, move more" is a practical fat loss strategy
- It also does not tell us what is driving changes in energy balance that cause obesity
Since energy balance is by far the main factor that determines body fat stores, naturally obesity researchers have been interested in what determines energy intake and energy expenditure, the two control points of energy balance, and there has been a tremendous amount of research into this in the last century. Now we come to the second reason why Taubes's argument is a red herring. He suggests that obesity researchers are in the wrong paradigm because they are focused on energy balance rather than the determinants of energy balance (e.g, they have the causality backward), but this is simply not true. Taubes states (57):
If the post-WW2 generation of researchers had simply defined obesity as a disorder of excess fat accumulation rather than one of energy balance, I argued, they would have naturally asked the question, what hormones and enzymes and other factors regulate fat accumulation. And that’s what they would have and should have been studying for the past sixty years.Someone should tell Gary Taubes about leptin. And after that, tell him about melanocortins, neuropeptide Y, dopamine, opioids, amylin, ghrelin and all the other factors that researchers have determined regulate body fat accumulation since WWII. Then, all of the brain regions that respond to these factors and have well-defined roles in body fat regulation (e.g., the arcuate nucleus, ventromedial hypothalamus, lateral hypothalamus, paraventricular nucleus of the hypothalamus). Just because these mechanisms involve the brain doesn't mean we get to pretend they don't exist, and then complain that no one is studying the question. Most obesity researchers view energy imbalance as a link in the causal chain between environmental factors and obesity, and view the whole process as being driven by upstream causal factors, just as Taubes does. That may not be reflected on TV or in the newspaper, but I can assure you it is a common sentiment in my field. There is no "paradigm shift" necessary here, because most obesity researchers already share Taubes's view on this-- in fact, they had already studied it in detail long before he came to town. And his statement that obesity researchers don't define obesity as a disorder of excess fat accumulation is simply absurd. There is no rational justification for brushing aside 60 years of obesity research on these grounds, but of course, agreeing with people is not very exciting.
The remaining two questions are, 1) where do the control points for energy intake and energy expenditure reside? 2) what causes energy imbalance?
The efforts of many dedicated researchers over the last century have uncovered a complex control system in the brain that adjusts energy intake and expenditure both in the short and long term to try to achieve stability (homeostasis) of body energy status over time. This system is composed of negative feedback loops between the digestive system and the brain for the control of meal-to-meal energy intake, and negative feedback loops between fat mass and the brain for the control of long-term energy balance and thus fat mass (58). This makes sense, since energy intake obviously involves the brain directing food seeking and ingestion, and energy expenditure involves the brain moving the body and controlling the sympathetic nervous system and thyroid signaling. There is no known system in fat tissue that would allow it to intrinsically regulate its own size with any degree of precision, nor is there any known system in the insulin-secreting pancreas that could do so. These organs do not appear to be a control point of energy balance or total body fat mass.
Now we are left with the question of what causes energy imbalance. We are looking for factors that influence the control systems in the brain that regulate energy balance and fat mass. Some good candidates have been identified, and I posted a summary of my thoughts on them recently (59).
To summarize the key points of this post:
- Energy balance tightly determines fat mass
- Energy balance is an extremely useful logical framework for obesity research
- This does not necessarily imply that "eat less, move more" is an effective fat loss strategy in practice
- The control point for energy balance appears to reside in the brain
- It is therefore likely that the causes of obesity influence this control system in the brain
Here, the body is running things. Indeed the organ in control may be the fat tissue itself in concert with the liver. The University of Vienna endocrinologist/geneticist Julius Bauer described this fat-rules concept back in 1929 by saying that the fat tissue of someone who’s obese (what he called “abnormal lipophilic tissue) “maintains its stock, and may increase it independent of the requirements of the organism. A sort of anarchy exists; the adipose tissue lives for itself and does not fit into the precisely regulated management of the whole organism.”
In this scenario, the brain plays no more role in regulating the growth of the fat tissue than it would regulating the growth of any tissue.I thought Taubes's idea is that insulin regulates fat tissue size? That means the pancreas would be in charge ("pancreas rules"), not the fat tissue itself. I'm pretty sure Dr. Bauer didn't sign up for "pancreas rules". But let's put that aside for now. Taubes left out a second quote by Dr. Bauer that is relevant here:
“The genes responsible for obesity act upon the local tendency of the adipose tissue to accumulate fat (lipophilia) as well as upon the endocrine glands and those nervous centers which regulate lipophilia and dominate metabolic functions and the general feelings ruling the intake of food and the expenditure of energy. Only a broader conception such as this can satisfactorily explain the facts.”Dr. Bauer was speculating here, because this was long before we had the tools to answer these questions directly-- today we know that the bold portion of his statement has received the most consistent scientific support (discussed in 61). It appears that even during those golden years of pre-WWII obesity research, before we had discovered leptin, before we understood in detail how the brain regulates body fatness, when obesity research was still taking its first baby steps-- even then, it was clear that the brain regulates body fat mass by controlling food intake and energy expenditure. Where did I get that quote? A book called Good Calories, Bad Calories, page 362 (thanks Evelyn).
At this point, I feel I've already spent too much time engaging Taubes, so I won't continue to do so. But I hope I've been able to convey some interesting obesity research to Whole Health Source readers during this process.