Does high protein explain the low-carb "metabolic advantage"?

In 2012, David Ludwig's group published a paper that caused quite a stir in the diet-nutrition world (1).  They reported that under strict metabolic ward conditions, weight-reduced people have a higher calorie expenditure when eating a very low carbohydrate diet (10% CHO) than when eating a high-carbohydrate diet (60% CHO)*.

In other words, the group eating the low-carb diet burned more calories just sitting around, and the effect was substantial-- about 250 Calories per day.  This is basically the equivalent of an hour of moderate-intensity exercise per day, as Dr. Ludwig noted in interviews (2).  The observation is consistent with the claims of certain low-carbohydrate diet advocates that this dietary pattern confers a "metabolic advantage", allowing people to lose weight without cutting calorie intake-- although the study didn't actually show differences in body fatness.

In Dr. Ludwig's study, calorie intake was the same for all groups.  However, the study had an important catch that many people missed: the low-carbohydrate group ate 50 percent more protein than the other two groups (30% of calories vs. 20% of calories).  We know that protein can influence calorie expenditure, but can it account for such a large difference between groups?

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Recent Interviews

For those who don't follow my Twitter account (@whsource), here are links to my two most recent interviews.

Smash the Fat with Sam Feltham.  We discuss the eternally controversial question, "is a calorie a calorie"?  Like many other advocates of the low-carbohydrate diet, Feltham believes that the metabolic effects of food (particularly on insulin), rather than calorie intake per se, are the primary determinants of body fatness.  I explain the perspective that my field of research has provided on this question.  We also discussed why some lean people become diabetic.  Feltham was a gracious host.

Nourish, Balance, Thrive with Christopher Kelly.  Kelly is also an advocate of the low-carbohydrate diet for fat loss.  This interview covered a lot of ground, including the insulin-obesity hypothesis, regulation of body fatness by the leptin-brain axis, how food reward works to increase calorie intake, and the impact of the food environment on food intake.  I explain why I think proponents of the insulin-obesity hypothesis have mistaken association for causation, and what I believe the true relationship is between insulin biology and obesity.  Kelly was also a gracious host.  He provides a transcript if you'd rather read the interview in text form.

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Thoughts on the McDougall Advanced Study Weekend

For those of you who aren't familiar with him, Dr. John McDougall is a doctor and diet/health advocate who recommends a very low fat, high starch, whole food vegan diet to control weight and avoid chronic disease.  He's been at it for a long time, and he's a major figure in the "plant-based diet" community (i.e., a diet including little or no animal foods).

Dr. McDougall invited me to participate in his 3-day Advanced Study Weekend retreat in Santa Rosa, CA.  My job was to give my talk on insulin and obesity, and participate in a panel discussion/debate with Dr. McDougall in which we sorted through issues related to low-carb, Paleo, and the health implications of eating animal foods.  I was glad to receive the invitation, because I don't see myself as a diet partisan, and I believe that my evidence-based information is applicable to a variety of diet styles.  I saw the Weekend as an opportunity to extend my thoughts to a new community, challenge myself, and maybe even learn a thing or two.  It was particularly interesting to compare and contrast the Advanced Study Weekend with the Ancestral Health Symposium, which is more Paleo- and low-carb-friendly.

General Observations

The attendees were a lot older than AHS attendees.  I estimate that most of them were in their 60s, although there were some young people in attendance.

I don't place too much emphasis on peoples' personal appearance at conferences like this.  You don't know what a person's background, genetics, or personal struggles may be, you don't know how closely they adhere to the program, and you don't know to what degree a group of people might be self-selected for particular traits*.  But I will note that Dr. McDougall, his family, and many of the other starch-based/plant-based diet advocates tended to be extremely lean with low fat and muscle mass.  They also tended to have a healthy and energetic appearance and demeanor.  As I would expect, decades of exceptionally high starch intake hasn't made them obese or obviously ill.

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What about the Other Weight Loss Diet Study??

The same day the low-fat vs low-carb study by Bazzano and colleagues was published, the Journal of the American Medical Association published a meta-analysis that compared the effectiveness of "named diet programs".  Many people have interpreted this study as demonstrating that low-carbohydrate and low-fat diets are both effective for weight loss, and that we simply need to pick a diet and stick with it, but that's not really what the study showed.  Let's take a closer look.

Johnston and colleagues sifted through PubMed for studies that evaluated "named diet programs", such as Ornish, Atkins, LEARN, Weight Watchers, etc (1).  In addition, the methods state that they included any study as low-carbohydrate that recommended less than 40% of calories from carbohydrate, was funded by the Atkins foundation, or was "Atkins-like".  These criteria weren't extended to the low-fat diet: only studies of name-brand low-fat diets like the Ornish diet were included, while the meta-analysis excluded low-fat diet studies whose guidelines were based on recommendations from government and academic sources, even though the latter group represents the majority of the evidence we have for low-fat diets.  The inclusion criteria were therefore extremely asymmetrical in how they represented low-carb and low-fat diets.  This fact explains the unusual findings of the paper.

The abstract immediately activated my skeptic alarm, because it states that at the one-year mark, low-carbohydrate diets and low-fat diets both led to a sustained weight loss of about 16 pounds (7.3 kg).  Based on my understanding of the weight loss literature, that number seems far too high for the low-fat diet, and also too high for the low-carbohydrate diet.

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Low-carbohydrate vs. Low-fat diets for Weight Loss: New Evidence

A new high-profile study compared the weight loss and cardiovascular effects of a low-carbohydrate diet vs. a low-fat diet.  Although many studies have done this before, this one is novel enough to add to our current understanding of diet and health.  Unlike most other studies of this nature, diet adherence was fairly good, and carbohydrate restriction produced greater weight loss and cardiovascular risk factor improvements than fat restriction at the one-year mark.  Yet like previous studies, neither diet produced very impressive results.

The Study

Lydia A. Bazzano and colleagues at Tulane University randomly assigned 148 obese men and women without cardiovascular disease into two groups (1):

1. Received instructions to eat less than 40 grams of carbohydrate per day, plus one low-carbohydrate meal replacement per day.  No specific advice to alter calorie intake.  Met regularly with dietitians to explain the dietary changes and maintain motivation.
2. Received instructions to eat less than 30 percent of calories from fat, less than 7 percent of calories as saturated fat, and 55 percent of calories from carbohydrate, plus one low-fat meal replacement per day.  No specific advice to alter calorie intake.  This is based on NCEP guidelines, which are actually designed for cardiovascular risk reduction and not weight loss.  Met regularly with dietitians to explain the dietary changes and maintain motivation.

Participants were followed up for one year, with data reported for 3 month, 6 month, and 12 month timepoints.  This study actually measured body fat percentage, but unfortunately did so using bioelectrical impedance (like on some bathroom scales), which is essentially meaningless in this context.

Results

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Fat and Carbohydrate: Clarifications and Details

The last two posts on fat and carbohydrate were written to answer a few important, but relatively narrow, questions that I feel are particularly pertinent at the moment:

• Was the US obesity epidemic caused by an increase in calorie intake?
• Could it have been caused by an increase in carbohydrate intake, independent of the increase in calorie intake?
• Does an unrestricted high-carbohydrate diet lead to a higher calorie intake and body fatness than an unrestricted high-fat diet, or vice versa?
• Could the US government's advice to eat a low-fat diet have caused the obesity epidemic by causing a dietary shift toward carbohydrate?

However, those posts left a few loose ends that I'd like to tie up in this post.  Here, I'll lay out my opinions on the relationship between macronutrient intake and obesity in more detail.  I'll give my opinions on the following questions:

• What dietary macronutrient composition is the least likely to cause obesity over a lifetime?
• What dietary macronutrient composition is best for a person who is already overweight or obese?
• Is fat inherently fattening and/or unhealthy?

From the beginning

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Fat vs. Carbohydrate Overeating: Which Causes More Fat Gain?

Two human studies, published in 1995 and 2000, tested the effect of carbohydrate vs. fat overfeeding on body fat gain in humans.  What did they find, and why is it important?

We know that daily calorie intake has increased the US, in parallel with the dramatic increase in body fatness.  These excess calories appear to have come from fat, carbohydrate, and protein all at the same time (although carbohydrate increased the most).  Since the increase in calories, carbohydrate, fat, and protein all happened at the same time, how do we know that the obesity epidemic was due to increased calorie intake and not just increased carbohydrate or fat intake?  If our calorie intake had increased solely by the addition of carbohydrate or fat, would we be in the midst of an obesity epidemic?

The best way to answer this question is to examine the controlled studies that have compared carbohydrate and fat overfeeding in humans.

Horton et al.

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Glucagon, Dietary Protein, and Low-Carbohydrate Diets

Glucagon is a hormone that plays an important role in blood glucose control.  Like insulin, it's secreted by the pancreas, though it's secreted by a different cell population than insulin (alpha vs. beta cells).  In some ways, glucagon opposes insulin.  However, the role of glucagon in metabolism is frequently misunderstood in diet-health circles.

The liver normally stores glucose in the form of glycogen and releases it into the bloodstream as needed.  It can also manufacture glucose from glycerol, lactate, and certain amino acids.  Glucagon's main job is to keep blood glucose from dipping too low by making sure the liver releases enough glucose.  There are a few situations where this is particularly important:

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Dogs Eating Carbs

Five years ago, I had an interesting conversation with a veterinarian friend about dog food.  We were talking about diabetes in one of the dogs she was treating, and I remarked "that's what happens when you feed a carnivore carbohydrate".  She gave me a funny look.  At the time, I was seeing the world through the low-carb lens, and I remember thinking how bizarre it was that she didn't yield to my impeccable logic.  As they say, live and learn.

The journal Nature published a fascinating paper on the evolution of the domestic dog today (1).  Researchers compared the genome of wolves and domestic dogs to see what genetic changes accompanied domestication.

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The Potato Diet

In 2010, I wrote a series of blog posts on the health properties of potatoes (1, 2, 3).  The evidence showed that potatoes are non-toxic, filling per calorie, remarkably nutritious, and can be eaten as almost the sole source of nutrition for extended periods of time (though I'm not recommending this).  Traditional South American cultures such as the Quechua and Aymara have eaten potatoes as the major source of calories for generations without any apparent ill effects (3).  This is particularly interesting since potatoes are one of the highest glycemic and most insulin-stimulating foods known.

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Nutrition Science Initiative (NuSI)

Some of you may have heard of an ambitious new nutrition research foundation called the Nutrition Science Initiative (NuSI).  In this post, I'll explain what it is, why it matters, and how I feel about it-- from the perspective of an obesity researcher. 

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Ancestral Health Symposium 2012

I recently returned from AHS12 and a little side trip to visit family.  The conference was hosted at Harvard University through the Harvard Food Law Society.  Many thanks to all the organizers who made it happen.  By and large, it went smoothly.

The science as expected ranged from outstanding to mediocre, but I was really encouraged by the presence and enthusiastic participation of a number of quality researchers and clinicians. The basic concept of ancestral health is something almost anyone can get behind: many of our modern health problems are due to a mismatch between the modern environment and what our bodies "expect".  The basic idea is really just common sense, but of course the devil is in the details when you start trying to figure out what exactly our bodies expect, and how best to give it to them.  I think our perspective as a community is moving in the right direction.

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Interview with Aitor Calero of Directo al Paladar

Aitor Calero writes for the popular Spanish cooking and nutrition blog, Directo al Paladar ("straight to the palate").  We did a written interview a while back, and he agreed to let me post the English version on my blog.  The Spanish version is here and here.

Without further ado, here it is:

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Why Did Energy Expenditure Differ Between Diets in the Recent Study by Dr. Ludwig's Group?

As discussed in the previous post, a recent study by Dr. David Ludwig's group suggested that during weight maintenance following fat loss, eating a very low carbohydrate (VLC) diet led to a higher metabolic rate (energy expenditure) than eating a low-fat (LF) diet, with a low glycemic index (LGI) diet falling in between the two (1).  The VLC diet was 30 percent protein, while the other two were 20 percent.  It's important to note that these were three dietary patterns that differed in many ways, and contrary to claims that are being made in the popular media, the study was not designed to isolate the specific influence of protein, carbohydrate or fat on energy expenditure in this context. 

Not only did the VLC diet lead to a higher total energy expenditure than the LF and LGI diets, the most remarkable finding is that it led to a higher resting energy expenditure.  Basically, people on the VLC diet woke up in the morning burning more energy than people on the LGI diet, and people on the LGI diet woke up burning more than people on the LF diet.  The VLC dieters burned 326 more calories than the LF dieters, and 200 more than the LGI dieters.

It's always tempting to view each new study in isolation, without considering the numerous studies that came before it, but in this case it's essential to see this study through a skeptical lens that places it into the proper scientific context.  Previous studies have suggested that:

1. The carbohydrate:fat ratio of the diet has little or no detectable impact on energy expenditure in people who are not trying to lose weight (2, 3).
2. The carbohydrate:fat ratio of the diet has little or no detectable impact on energy expenditure in people who are being experimentally overfed, and if anything carbohydrate increases energy expenditure more than fat (4, 5).
3. The carbohydrate:fat ratio of the diet has little or no detectable impact on energy expenditure during weight loss (6, 7, 8), and does not influence the rate of fat loss when calories are precisely controlled. 

This new study does not erase or invalidate any of these previous findings.  It fills a knowledge gap about the effect of diet composition on energy expenditure specifically in people who have lost weight and are trying to maintain the reduced weight.

With that, let's see what could have accounted for the differences observed in Dr. Ludwig's study.
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New Study: Is a Calorie a Calorie?

A new study in JAMA led by Dr. Cara B. Ebbeling and colleagues purports to challenge the idea that all calories are equally fattening (1).  Let's have a look.  When thinking about the role of calorie intake in body fatness, there are basically three camps:

1.    Calories don’t matter at all, only diet composition matters.
2.    Calories are the only thing that matters, and diet composition is irrelevant.
3.    Calories matter, but diet composition may also play a role.

The first one is an odd position that is not very well populated.  The second one has a lot of adherents in the research world, and there’s enough evidence to make a good case for it.  It’s represented by the phrase ‘a calorie is a calorie’, i.e. all calories are equally fattening.  #1 and #2 are both extreme positions, and as such they get a lot of attention.  But the third group, although less vocal, may be closest to the truth. 
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What Causes Insulin Resistance? Part V

Previously in this series, we've discussed the role of cellular energy excess, inflammation, brain insulin resistance, and micronutrient status in insulin resistance.  In this post, I'll explore the role of macronutrients and sugar in insulin sensitivity.

Carbohydrate and Fat

There are a number of studies on the effect of carbohydrate:fat ratios on insulin sensitivity, but many of them are confounded by fat loss (e.g., low-carbohydrate and low-fat weight loss studies), which almost invariably improves insulin sensitivity.  What interests me the most is to understand what effect different carbohydrate:fat ratios have on insulin sensitivity in healthy, weight stable people.  This will get at what causes insulin resistance in someone who does not already have it.

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I Got Boinged, and Other News

The reaction to my post "The Carbohydrate Hypothesis of Obesity: a Critical Examination" has been overwhelmingly positive, particularly among the scientists I've heard from. 

On Saturday, the inimitable maker and writer Mark Frauenfelder posted a link to my post on the variety blog BoingBoing.  BoingBoing has been on my sidebar for three years, and it's the place I go when I need a break.  It's a fun assortment of science, news, technology and entertainment.  BoingBoing was originally a zine started by Frauenfelder and his wife in 1988, and it has been on the web since 1995.  Today, it has multiple contributing authors and it draws several hundred thousand hits per day.  I'm thrilled that Frauenfelder posted my article there.  Apparently he likes my blog.  Thanks!

I added a new section (IIB) to my original post.  It discusses what human genetics can teach us about the mechanisms of common obesity.  It is consistent with the rest of the evidence suggesting that body fatness is primarily regulated by the brain, not by fat tissue, and that leptin signaling plays a dominant role in this process. 

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The Carbohydrate Hypothesis of Obesity: a Critical Examination

Introduction

I'd like to begin by emphasizing that carbohydrate restriction has helped many people lose body fat and improve their metabolic health.  Although it doesn't work for everyone, there is no doubt that carbohydrate restriction causes fat loss in many, perhaps even most obese people.  For a subset of people, the results can be very impressive.  I consider that to be a fact at this point, but that's not what I'll be discussing here. 

What I want to discuss is a hypothesis.  It's the idea, championed by Gary Taubes, that carbohydrate (particularly refined carbohydrate) is the primary cause of common obesity due to its ability to elevate insulin, thereby causing increased fat storage in fat cells.  To demonstrate that I'm representing this hypothesis accurately, here is a quote from his book Good Calories, Bad Calories:

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Healthy Skeptic Podcast

Chris Kresser has just posted our recent interview/discussion on his blog The Healthy Skeptic.  You can listen to it on Chris's blog here.  The discussion mostly centered around body fat and food reward.  I also answered a few reader questions.  Here are some highlights:

• How does the food reward system work? Why did it evolve?
• Why do certain flavors we don’t initially like become appealing over time?
• How does industrially processed food affect the food reward system?
• What’s the most effective diet used to make rats obese in a research setting? What does this tell us about human diet and weight regulation?
• Do we know why highly rewarding food increases the set point in some people but not in others?
• How does the food reward theory explain the effectiveness of popular fat loss diets?
• Does the food reward theory tell us anything about why traditional cultures are generally lean?
• What does cooking temperature have to do with health?
• Reader question: How does one lose fat?
• Reader question: What do I (Stephan) eat?
• Reader question: Why do many people gain fat with age, especially postmenopausal women?

The podcast is a sneak preview of some of the things I'll be discussing in the near future.  Enjoy!

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Food Reward: a Dominant Factor in Obesity, Part III

Low-Fat Diets

In 2000, the International Journal of Obesity published a nice review article of low-fat diet trials.  It included data from 16 controlled trials lasting from 2-12 months and enrolling 1,910 participants (1).  What sets this review apart is it only covered studies that did not include instructions to restrict calorie intake (ad libitum diets).  On average, low-fat dieters reduced their fat intake from 37.7 to 27.5 percent of calories.  Here's what they found:
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