Diet, weight loss and body composition changes

This is an unfortunately long post, and I apologize for it, but the reason is that I find all this so darn interesting.  Hope you do to.

A little while back I looked closer at some of the science behind diet, weight loss and body re-composition. I have heard people say on several occasions that a low carbohydrate diet will prevent loss of muscle mass and that all weight lost is fat. So I wanted to find out once and for all what really happens with our body when we lose weight. I’ll show you some of the data, and although these studies are not the only ones, I am confident that the studies presented here give a satisfactory accurateness

So there is much debate about what happens to our body composition when we lose weight and perhaps especially when we do it using a low carbohydrate diet. This quote is from Sachiko T. et al 2001. Dietary Protein and Weight Reduction: A Statement for Healthcare Professionals From the Nutrition Committee of the Council on Nutrition, Physical Activity, and Metabolism of the American Heart Association:

Some popular high-protein/low-carbohydrate diets limit carbohydrates to 10 to 20 g/d, which is one fifth of the minimum 100 g/d that is necessary to prevent loss of lean muscle tissue.

Clearly the AHA suggests that we will lose muscle tissue by going low carb. In my school we used the exercise physiology textbook from McArdle, Katch and Katch (2007) which said this:

…low carbohydrate diet sets the stage for a significant loss of lean tissue as the body recruits amino acids from muscle to maintain blood glucose via gluconeogenesis.

Once again, low carbohydrate dieting does not seem a good idea if we want to preserve muscle mass while we lose fat mass.

But the questions remains unanswered; how much muscle mass do we lose if we go low carb and can we do anything to prevent a potential loss of muscle tissue?

Let us look at some studies and see what they tell us.

Studies
This study from Bonnie Brehm and coworkers compared a low carbohydrate diet to a low fat diet:

All participants in the above study were women and they were obese. Dietary energy content was reduced in both diets and body composition was measured using Dual Energy X-ray Absorptiometry (DEXA). As you can see, weight loss was greater with low carb, but so was loss of lean body mass (LBM) and the percentage loss of LBM was not much different between diets. 
Here’s another study:
This was a crossover study where all the participants tried two different diets in random order. The results are given under:
As is usually the case in weight loss trials, the men lost more weight than the women. And once again low carb caused a greater weight loss, but also quite the loss of lean body mass. The women eating low fat seemed to lose the greatest percentage LBM, which is also a recurrent theme in weight loss trials. 
Next, here’s Kelly Meckling and coworkers:
One of the goals in this study was for the low fat group to reduce their calorie intake to the naturally reduced level of the low carbers. Weight loss did not differ between groups, but loss of LBM was significantly larger in the low carb group and over 25% of the LC weight loss was lean body mass. Body composition was measured using bioelectrical impedance analysis (BIA).
Next, as study from William Yancy and coworkers from 2004:
  
Weight loss with low carb was double that of low fat and this time loss of fat free mass (FFM) was actually quite larger in the low fat group. LBM is what is left if we remove fat mass and skeletal mass. Fat free mass is, not surprisingly, total mass minus fat mass. LBM and FFM are used interchangeably. 
It seems that loss of non-fat mass is common, regardless of diet, but we need to look at some more studies to get a clearer picture.
Here’s one from down under, from Manny Noakes:
This is a short study, but with 83 participants. The results are pretty similar, both when it comes to weight and LBM loss, but in both diets around 30% of the lost weight was LBM and that is rather much.
Another one from Australia. Here’s Jennifer Keogh and coworkers:
Both diets were 30% energy restricted and designed to be isocaloric. Once again there was a significant loss of fat free mass with both diet strategies.
Jeff Volek brought us this study in 2008:
An Atkins type diet was compared to a regular calorie restricted low fat diet in 40 men and women. Weight loss was greater with low carb, but so was loss of LBM. So far, there seems to be little truth to any claim that low carb preserves LBM.
This next one is another crossover study:
Alexandra Johnstone and coworkers showed us yet again that weight loss is greater with low carb, but that so is loss of FFM. Notice that this is a study of men only and so the percentage loss of FFM is much smaller than in studies of women.
One last study. Third one from Australia, this time by Grant D. Brinkworth:
118 people participated in this eight week study and were scanned with DEXA. Weight loss was greater with low carb and both groups lost about 20% FFM.
To summarize, loss of fat mass is greater with LC than LF diets. Loss of LBM is common on both LF and LC diets, but as we will see, not obligate. But there are some considerations to make first.
Considerations
First of all, any loss of water will usually be considered LBM and so if there is a difference in water loss between diets, this will affect loss of LBM/FFM. Carbohydrate restriction usually does cause a greater loss of body water, at least in the initial phase of the diet. Loss of glycogen with low carb will cause a parallel loss of water and so there is reason to expect a larger loss of LBM with low carb, and we need to remember that LBM is not a measure of muscle proteins.  
Contradictory findings
Although loss of LBM is clearly common on low carb diets, there are studies suggesting that such a loss can be avoided.
In a very small crossover study by Benoit et al from 1965 we can see the obvious advantage of low carb dieting compared to fasting:
Notice the difference in LBM loss. One likely advantage of carbohydrate restriction is that the combination of adequate protein intake and high ketone body production spares muscle proteins from being used to produce glucose. The Benoit study is small, but it suggests that loss of LBM is not a necessary consequence of low carb dieting.
And look at this one:
In this study of twelve men, LBM increased during the diet period, even though there was no change in the exercise pattern of the subjects. It is results like these, which sometimes appear, that suggests that it is possible to lose weight in a way that spares muscle tissue. In another very small study of very obese adolescents, similar results were found:
After eight weeks of a very low calorie ketogenic diet, lean body mass increased by almost 1,5kg while 15kg of fat was lost.
So I think it’s time to ask what the difference between these few studies where LBM increases (in spite of water loss) and the RCT’s where a low carbohydrate diet always leads to some LBM loss. But remember also that not all LBM is functional LBM. That is, we expect some loss of LBM and some LBM can be lost without negative consequences. We must remember to keep our feet on the ground, there is no problem with some loss of LBM with large losses of fat mass.
To make a long story short, there are some important factors we can manipulate in order to reduce loss of LBM. Being a man is perhaps the most effective. Men lose more fat and less LBM when they lose weight. It’s just the way it is. But both men and women can increase their protein intake. In many of the RCT’s in this post, average protein intake was low, often around 1g/kg body weight/day. The optimal intake is probably closer to 1.8g/kg/day (severely overweight people should use ideal body weight instead of actual body weight).
Several studies have found a correlation between protein intake and LBM loss. James Krieger wrote this in 2006:
  
And he concluded thusly:
In a very recent review article, Stuart Philips and Luc van Loon has this to say:
The thing with carbohydrate restriction is that is causes a greater fat loss and greater LBM loss than low fat strategies, but the end result is that low carb thus causes a greater reduction in body fat percentage and so the greater change in body composition. To optimize the results, protein intake should most likely be kept at >1,5g/kg/day. Here’s another quote from Phillips and van Loon:

There is also the matter of sodium and potassium that might play a part in the results. Potassium is an important intracellular ion in our muscles and adequate potassium is important for creating an anabolic environment. The trouble with ketosis or severe carbohydrate restriction is that it causes our kidneys to excrete sodium and unless that sodium is properly replaced the kidneys compensate by excreting potassium. In short, when optimal body composition changes is the goal, or optimal performance, salt intake is important and should be a good deal higher than the daily recommended intake.

In addition to minding our protein and salt intake, we can of course also do resistance exercise in order to increase lean mass retention or even increase lean mass while reducing fat mass. It is, not surprisingly, well documented that resistance exercise, as a part of weight loss, is very effective at reducing lean mass loss, regardless of diet. But in order for resistance exercise to yield optimal results, protein and salt intake must be optimized.  
Richard Wood and coworkers just published results from a study where overweight older men were put on two different diets with or without resistance exercise. Here are the results:
Even though the results favor both low carbohydrate dieting and resistance exercise, I must say that I was surprised at the amount of FFM loss in the low carbohydrate and resistance exercise group, even when considering that some is water loss. After 12 weeks I would have suspected FFM to have increased. But there are once again some factors to consider. First of all, the mean age of the participants were 60 years. This may have caused the results to be smaller than if younger men participated. Also the resistance exercise was not very heavy, it could have been a good deal heavier and it is likely that muscle hypertrophy would then have been greater.
Donald K. Layman and coworkers compared the effects of two different diets varying in protein and carbohydrate content, with or without resistance exercise. The graphs on the left are women and the ones on the right are men:

Clearly, both increasing protein/decreasing carbohydrate and resistance exercise improve body composition changes. The low carbohydrate diet in this study was not very low. Average carb intake during the intervention was 141g in LC and 126g in LC+RE. Protein intake was 110g and 102g respectively.

I’d like to compare the results of a study I conducted in 2010 with that of a study from Donnely from 1991:

These are two very different strategies. In our study the participant were told to be in dietary ketosis, but could eat as much as they liked. In Donnely’s study calories was severely restricted. Also in our study the participants exercised twice a week, whereas in Donnely’s they exercised four times per week (resistance exercise). They are both effective strategies both for losing weight and changing body composition, so it is up to us what we prefer. I for one would like to eat as much as I please and not have to exercise that much to get the results I want.

The conclusion
Loss of LBM with weight loss is common but not obligate. A low carbohydrate diet is no grantee for all weigh loss being fat. In order to achieve optimal body re-composition one should reduce carbohydrates, make sure to eat enough protein and salt, and do regular heavy resistance exercise. The results one can achieve are quite astonishing.

The satiating effects of protein

«The mechanisms by which protein may affect satiety remain elusive.» 

Halton and Hu 2004 [1]

“Although the immediate satiating effect of dietary fat may be comparatively weak, there is no doubt that ingested fat does inhibit feeding.” 

Leonhardt 2004 [2]

LCHF opponents keep throwing out the same old argument, that fat is the least satiating macronutrient and that all that fat might thus make people hungry and unable to stay with the strategy. Eventually the low satiating effect of fat will cause people to gain weight. This is claimed despite the existence of several studies showing that people put on ad libitum high fat diets experience less hunger, lose weight and all over seem perfectly fine.

Protein, it is said, is the most satiating macronutrient. So the best dietary strategy is replacing fat with proteins and keeping carbs high.

My colleagues in dispute seem very eager to have me agree that protein is very satiating and that we at least should have this as common ground.

But my own experience urges me not to agree. If I reduce my fat intake and eat more protein, as I sometimes do, for example in periods of stress where I eat too much eggs and lean meat and forget about the fat, I feel horrible. My blood sugar drops and over time lethargy hits in. What’s more, I soon feel hungry and start craving fat/carb combos. Simply eating fat eases my symptoms. Eating carbohydrates would probably also ease my symptoms, but we all know that is no good long term solution.

So are proteins especially satiating?

Weigle et al [3] placed 19 subjects sequentially on the following diets: a weight-maintaining diet (15% protein, 35% fat, and 50% carbohydrate) for 2 wk, an isocaloric diet (30% protein, 20% fat, and 50% carbohydrate) for 2 wk, and an ad libitum diet (30% protein, 20% fat, and 50% carbohydrate) for 12 wk.

Weigle is good for a laugh. Here’s from the introduction of the article

“Both low-fat diets (2– 4) and low-carbohydrate diets that are high in fat and protein have been shown to cause a decrease in ad libitum caloric intake and significant weight loss in humans. Thus, it appears that diets with fat contents at opposite extremes have the same therapeutic result, despite evidence that excessive dietary fat intake promotes obesity. This paradox could be explained if it is the high protein content rather than the lower carbohydrate content of low-carbohydrate diets that offsets the deleterious effect of high fat intakes and results in weight loss.” 

Quite the paradox there. Hope someone will resolve it someday. 

Weigle is often cited for showing that proteins are satiating. But measurements of hunger and fullness showed that even though hunger was reduced and fullness increased during the isocaloric diet, they returned to baseline with the ad libitum diet despite constant protein content. The reason the study is sited is because calorie intake dropped with higher protein. However, satiety and calorie intake did not seem to correlate. 
As in all similar studies, the high protein diet differed from the low protein diet in many aspects even though carbohydrate intake remained constant. Below is an example of what the two different diets might contain. 

So can we conclude that the hunger (temporarily) and body weight dropped because of the higher protein content? Of course not. That would be silly. It might be the proteins, but it might be any one of the other differing dietary factors.

Weigle and colleagues also wrote that

“It is likely that a reduction in dietary fat by 15% of total energy contributed to weight loss in the present study.”

This is a very strange thing to claim, as several studies where subjects are put on high fat diets reports significant weight loss and reduced hunger.

Weigle concluded thusly

“An increase in dietary protein from 15% to 30% of energy at a constant carbohydrate intake produces a sustained decrease in ad libitum caloric intake that may be mediated by increased central nervous system leptin sensitivity and results in significant weight loss. This anorexic effect of protein may contribute to the weight loss produced by low-carbohydrate diets.” 

Skov et al [4] randomized 65 subjects to two ad libitum fat reduced (30%) diets for six months. One with 12% energy from protein and one with 25% from protein. Weight loss in the low protein group was 5.1kg and 8.9kg in the high protein group. By labeling the diet higher in protein a “high protein diet” our focus is drawn away from the fact that the high protein diet also had significantly less carbohydrates. This is a recurring problem; how should the diets be labeled? The labeling wouldn’t actually be problem if the researchers remembered to properly discuss the effects of reduced carbohydrate intake or reduced glycemic index. This, however, is often not done and when a diet labeled “high protein diet” is discussed the protein content usually get the major part of the attention.

Skov and his Danish research fellows later wrote that

“The mechanisms responsible for the larger weight loss caused by an HP diet may be attributed to a greater satiety and fullness, and also the thermogenic effect of protein.” 

But of course, they might be right. A number of studies have compared hunger and satiety in the hours following consumption of a single meal, and have come to the conclusion that a high-protein meal is more satiating. So to say that a high protein diet suppresses hunger might be a correct statement, but it’s still a bloody unfair statement. Because what matters is the long term effect on hunger, and what actually cause the decreased hunger. The studies looking at single meal effects are usually poorly controlled and there are many confounding factors. Also, the protein content of high protein meals is often very high, ranging from 40% to 75%, and most of the studies have very few participants.

One of these studies, from Stubbs et al [5] (60% protein), found that there was no difference in subsequent energy intake despite acutely reduced hunger following a high protein meal. This was one of the more well controlled single meal studies.

Thomas Holton [1] notes that

“There are, however, some methodological issues concerning this type of research. Satiety appears to be influenced by a wide variety of factors including palatability, food mass, energy density, fiber and glycemic index. When using real foods, it is difficult if not impossible to control for all of these influences at the same time while still delivering different amounts of protein.” 

Fat is often considered the least satiating macronutrient from these single meal studies. But it might not be that simple. Mark I Friedman found that hepatic ATP, or the energy availability of the liver, exerts a strong effect on feelings of hunger. What is important, is that there’s fuel available, be it glucose or fat. A theoretical satiating effect of proteins is their conversion to glucose by gluconeogenesis thus providing more fuel for the liver.

A quote from Friedman

“Hyperphagia associated with the development of obesity is accompanied by a metabolic state that fosters the deposition of fat in adipose tissue, the largest fuel storage compartment. This shift in fuel partitioning toward storage is independent of and occurs before the change in food intake in nearly every animal model studied. According to the model presented here, overeating results because fuels that would otherwise be oxidized to produce ATP in a detectable manner are redirected into fat stores.” [6] 

And what redirects fuel into fat stores? I’ll leave it to you to figure this one out yourself. The point is that according to Friedman’s work, a higher fat diet will reduce hunger by making both glucose and fat more available for oxidation.

Daniel H. Bessesen [7] also believes that what separates obesity prone and those prone to leanness are differences in the trafficking of fat. He writes

“It may be that a preferential delivery of dietary fat to metabolically active tissues including liver and skeletal muscle allows more accurate sensing of dietary fat in a manner that promotes more accurate coupling between dietary fat intake and oxidation. Conversely, preferential delivery of dietary fat to adipose tissue may impair nutrient sensing and promote weight gain.” 

On low carb ketogenic diets, hunger is often drastically reduced within a matter of a few days after initiation of carb restriction. With fasting or starvation we see a drop in hunger with increased ketone body concentration. This satiating effect is often attributed to the ketone bodies themselves, in particular beta-hydroxybutyrate, but according to Friedman’s theory it could just as likely be caused by the increased internal energy availability that occurs when lipolysis and fat oxidation (with a subsequent increased ketone body production) are increased. 

Some studies also suggest that you will experience a stronger hunger if you eat some food as mostly carbs, than if you eat no food at all. 
The belief that high protein diets are especially satiating seem similar to the belief that high fat diets are fattening. Of course they might be, but as I said, it would be a bloody unfair statement. In animal studies high fat diets often do cause obesity, but normally only in the presence of a substantial amount of carbohydrates (or crazy amounts of frankenfats). The term “high fat diet” does not imply minimal carbohydrates. High protein diets might decrease hunger, but higher protein diets are usually lower in carbohydrates, sugars and have a lower glycemic index. Attributing the decreased hunger to the proteins might be just as much off target as attributing weight gain to fat.

Halton and Hu illustrates this point when they term many low carb study diets, high protein, low carb diets. Like the much sited study by Samaha et al [8]. In this study the low carb diet was a 1630kcal, 22% protein, 41% fat and 37% carbohydrate diet. Protein intake was well below 1g per kilo body weight. It produced a greater weight loss than a 1576kcal, 16% protein, 51% carbohydrate and 33%fat diet. The results can hardly be attributed to the proteins alone. Holtan and Hu, in their review of high protein diets and satiety, forget to discuss the potential long term satiating effects of increased fat intake.

Monika Leonhardt [2] seem more open and writes

“Fat seems to be less satiating than carbohydrate and might therefore lead to passive overconsumption [4]. Yet, in rodents, the efficacy of a high-fat diet to induce hyperphagia appears to be related to the energy and carbohydrate content of the diet. Therefore, overeating of high-fat diets is presumably not due to the high fat content alone. This assumption is in line with recent studies in humans showing that a high-fat, low-carbohydrate diet reduced rather than increased voluntary energy intake.” 

Leonhardt continues to suggest that overeating on a high fat diet might be, amongst others, due to

“the high energy density of such diets in combination with their carbohydrate content” 

“the usually low postprandial oxidation of ingested fat in the presence of carbohydrates.”

That protein exerts some acute satiating effect compared to carbohydrate and fat is hardly a good point. It is an interesting observation, but not an argument in favor of high protein diets. People put on high fat low carbohydrate diets also feel their hunger disappear and shed weight without caloric restriction. The high protein diets seem to stem from the cognitive dissonance of the upholders of the traditional dietary dogma. First fat was fattening, now it seems carbs are equally so. What they are left with are diets low in both fat and carbohydrates, diets that do not consider any of the important roles of the vast variety of fatty acids available to the body. I’ll eat my hat the day some anthropologist can show me a traditional human population thriving on a high protein, low fat, low carbohydrate diet. Fat matters.

References

1. Halton TL, Hu FB: The effects of high protein diets on thermogenesis, satiety and weight loss: a critical review. J Am Coll Nutr 2004, 23: 373-385.

2. Leonhardt M, Langhans W: Fatty acid oxidation and control of food intake. Physiol Behav 2004, 83: 645-651.

3. Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, Purnell JQ: A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr 2005, 82: 41-48.

4. Skov AR, Toubro S, Ronn B, Holm L, Astrup A: Randomized trial on protein vs carbohydrate in ad libitum fat reduced diet for the treatment of obesity. Int J Obes Relat Metab Disord 1999, 23: 528-536.

5. Stubbs RJ, van Wyk MC, Johnstone AM, Harbron CG: Breakfasts high in protein, fat or carbohydrate: effect on within-day appetite and energy balance. Eur J Clin Nutr 1996, 50: 409-417.

6. Friedman MI: Control of energy intake by energy metabolism. Am J Clin Nutr 1995, 62: 1096S-1100S.

7. Bessesen DH: Update on obesity. J Clin Endocrinol Metab 2008, 93: 2027-2034.

8. Samaha FF, Iqbal N, Seshadri P, Chicano KL, Daily DA, McGrory J, Williams T, Williams M, Gracely EJ, Stern L: A low-carbohydrate as compared with a low-fat diet in severe obesity. N Engl J Med 2003, 348: 2074-2081.