Low Carbohydrate Diets for Weight Loss: A brief review for Les Mills International Ltd

September 2012
Compiled by: Jennifer Fleming, MS, RD

Introduction
Dietary approaches that promote weight loss, decrease obesity related diseases and are
acceptable for life-long use have been the focus of much debate over the past several decades. In
the early 2000s low carbohydrate diets the rage. These days their popularity among the general
public wavers, but the behind the scenes scientific battle to determine the safety and efficacy of
these diets continues. Low carbohydrate diets derive a large portion of their energy intake from
protein and fat, and there is concern for the potential detrimental effects this may have on blood
lipid levels and cardiovascular disease risk. Thus, basic, clinical, and epidemiological research
on reduced carbohydrate dietary patterns continues to grow, evaluating the impact of this way of
eating on weight loss, obesity related diseases and the development of adverse effects.
Numerous randomized controlled dietary weight loss trials conducted over the past
several years reinforce the initial findings that reduced carbohydrate diets promote greater shortterm (< 6 months) weight loss than low-fat calorie restricted diets (Foster et al., 2003; Samaha et
al., 2003; Brehm et al.,, 2003; Yancy et al., 2004; Gardner et al., 2007). However, a small group
of studies that have extended the follow-up to one year did not show this effect (Foster et al.,
2003, Due et al., 2004; Das et al., 2007; Stern et al., 2004; Dansinger et al., 2005). Because of
the substantial controversy regarding low-carbohydrate diets, and even disagreements in
interpreting the results of specific studies, it has proven difficult to objectively summarize the
research in a way that reflects scientific consensus. In many cases small sample sizes, lack of
adherence data to assigned diets, and a large loss to follow-up limit the interpretation of a large
majority of weight-loss trials.
This review therefore will examine the most directly relevant scientific studies, which
having occurred largely in the 2000s. Supporters and opponents of low-carbohydrate diets
frequently cite many articles (sometimes the same articles) as supporting their positions. One of
the fundamental criticisms of those who advocate the low carbohydrate diets has been the lack of
long-term studies evaluating their health risks. However, as presented in this review, this has
begun to change as long term studies are readily emerging.
Summary
A search of the literature using PubMed reveals nearly 2000 published articles on the use
of a low carbohydrate diet for weight loss. As early as 2002, sources had already concluded that
2

much scientific and anecdotal evidence demonstrates favorable metabolic responses to low
carbohydrate diets (Volek & Westman, 2002). Despite this, both supporters and opponents
continued to investigate the topic seeking additional evidence to substantiate their beliefs. In this
paper the goal will be to exhaust the literature and seek clarity about whether the macronutrient
distribution of the diet is a determinant of weight loss. Literature will be reviewed to find
relevant studies and elaborate on the health implications of a low carbohydrate (high protein,
high fat) diet, specifically looking at weight loss and the effect on risk factors for cardiovascular
disease and diabetes.
The main arguments to support the use of low carbohydrate diets is the claim that the
metabolic changes that occur with a reduction in carbohydrate intake promotes more rapid
weight loss (Volek & Westman, 2002). While others suggest that the high protein, low
carbohydrate diet provides better satiety, resulting in a lower calorie intake and successful weight
loss. In contrast, opponents believe that when weight loss occurs with a low carbohydrate diet, it
is a result of a calorie deficit and/or increase in activity level (Bravata et al., 2003), which can be
acheived through a variety of dietary patterns.
Defining the Low Carbohydrate Diet
Diets that limit carbohydrate intake have been called low carbohydrate, very low
carbohydrate, high protein, high fat, and ketogenic diets. For the purpose of this review, the term
low carbohydrate diet will be defined as <130 g of carbohydrate per day. This is based on the
American Diabetes Association definition. However, it must be noted that some studies included
in this review do not meet this standard and have been identified as such in the summary table.
As a point of reference, 130 g carbohydrate equals 43% of calories in a 1,200-calorie diet, 30%
of calories in a 1,700-calorie diet, or 24% of calories in a 2,200-calorie diet.
Studies include a broad range of dietary carbohydrate content, as a result of varying
calorie recommendations, and assess the effect of carbohydrate restriction on the outcomes of
weight loss, blood levels of triglycerides (TG), low-density lipoprotein cholesterol (LDL-C),
high-density lipoprotein cholesterol (HDL-C), total cholesterol (TC), and glycemic control using
glycosylated hemoglobin A1c (HbA1c) and/or fasting glucose. It is important to understand that
there is no clear cut definition of a low carbohydrate diet in the literature. Various popular diets

recommend carbohydrate intakes of < 20% of caloric intake with absolute amounts of < 5060
gm/day, sometime as low as 2030 gm/day at least for short periods.
The caloric deficit due to carbohydrate restriction may be balanced with increased intake
of proteins and fats although the distribution is not always clear in the application of popular
diets and, in several studies, no increase in dietary intake of proteins or fats was observed
presumably due to effect of the low carbohydrate diet on appetite and satiety (Foster et al., 2003;
Samaha et al., 2003; Yancy et al., 2005). It is interesting that despite advocating ad libitum fat
and protein intake, a low carbohydrate diet may be hypocaloric either by design or by
spontaneous reduction of intake (Boden et al., 2005).
The Position of Medical Organizations
While the majority of the medical community remains somewhat opposed to low
carbohydrate diets (as defined as < 130 g carbohydrate per day or < 35% total calories from
carbohydrate) for long term health there has been a recent softening of this opposition by
organizations such as the American Diabetes Association.
In 2008 Shai et al., studied 322 moderately obese adults over a 2-year period assigning
each to one of three diets: a low-calorie, low fat diet (based on the 2000 AHA recommendations
of 30% total fat, with 1500 kcal for women and 1800 kcal for men,); a low-calorie Mediterranean
diet (1500 kcal for women, 1800 kcal for men, up to 35% total fat); or a low carbohydrate diet
based on the Atkins diet approach (20 g/day for two months with a gradual increase to a
maximum of 120 g/day, calories unrestricted). Participants in the low carbohydrate group were
counseled to choose vegetarian sources of fat and protein and to avoid trans fat. The results
showed that the low carbohydrate group had both the greatest weight loss and greatest
improvement in lipids (cholesterol). The Mediterranean group showed the greatest improvement
in glycemic control (related to diabetes). The authors concluded that personal preferences and
metabolic considerations might inform individualized tailoring of dietary interventions.
Interestingly, this study was significant enough that the American Heart Association
issued an immediate response to clarify its position (essentially saying that the low fat diet used
in the study is no longer recommended by the AHA). In addition, the American Diabetes
Association revised their Nutrition Recommendations and Interventions for Diabetes in 2008 to
acknowledge low carbohydrate diets (< 130 g carbohydrate) as a legitimate weight-loss plan.
4

While the recommendation falls short of endorsing low carbohydrate diets as a long-term health
plan, this was the first statement of supportalbeit for the short-termby one of the foremost
medical organizations. In its 2009 publication of Clinical Practice Recommendations, The ADA
again reaffirmed its acceptance of carbohydrate-controlled diets as an effective treatment for
short-term (up to one year) weight loss among obese people suffering from type 2 diabetes.
In contrast, the Academy of Nutrition and Dietetics has remained steadfast in their belief
that "there is no magic bullet to safe and healthful weight loss. The Academy continues to
endorse the high carbohydrate diet recommended by the National Academy of Sciences (180-230
g/day for females; 220-330 g/day for males; or 45-65% of total calories from carbohydrate).
They have recently stated: "Calories cause weight gain. Excess calories from carbohydrates are
not any more fattening than calories from other sources. Despite the claims of low carbohydrate
diets, a high carbohydrate diet does not promote fat storage by enhancing insulin resistance.
Likewise, the American Heart Association does not recommend high protein (low
carbohydrate) diets. The Association continues to hold the belief that such diets are associated
with increased risk for coronary heart disease. Other medical organizations such as the Canadian
Heart and Stroke Foundation and the UK Food Standards Agency hold similar views. The US
Department of Health and Human Services does not promote the use of low carbohydrate diets
for long term weight maintenance or heart health.
Weight loss
Low carbohydrate dietary patterns continue to be studied for their effect on weight loss.
This review includes trials conducted with heterogeneous populations and with variable
prescriptions of macronutrient content and calorie restriction. For example, a 24-week
randomized trial of an isocaloric very low carbohydrate diet (< 4% carbohydrate; average intake
1603 kcal/d) and a high-carbohydrate, low-fat diet (46% carbohydrate; average intake 1529
kcal/d) in nondiabetic abdominally obese individuals found comparable weight loss in both
groups (Tay et al., 2008). Westman et al. 2008 conducted a similar 24-week randomized trial
comparing a low carbohydrate diet [prescribed intake < 20 g of carbohydrate daily; actual intake
49 13 g (13% of daily caloric intake)] to a low glycemic index diet (actual intake 44%
carbohydrate) in 81 obese individuals with type 2 diabetes. Participants in the low carbohydrate
diet group lost more weight than those on the low glycemic index diet (11.1 8.73 kg vs 6.9
5

8.31 kg) in spite of higher caloric intake and comparable physical activity levels. Gardner et al.
(2007) randomized 311 premenopausal women to one of four diets: Atkins low carbohydrate diet
(20g/d or less carbohydrate for 2-3 months followed by increase to 50 g/d), Ornish diet (no more
than 10% calories from fat), LEARN diet (prudent diet of 55-60% carbohydrate and less than
10% saturated fat), and the Zone diet (40%-30%-30% distribution of carbohydrate, protein, and
fat). At the end of 1 year they found that those randomized to the Atkins low carbohydrate diet
lost the most weight (-4.7 1.6 kg) despite similar energy intakes at all time points compared
with participants following the Ornish (-2.6 1.2 kg), LEARN (Lifestyle, Exercise, Attitudes,
Relationships, and Nutrition; -2.2 1.4 kg), or Zone (-1.6 1.2 kg) diets.
Two trials published in 2008 and 2009 evaluated the effect of reduced carbohydrate
intake on weight loss over a period of 2 years. In 2008, Shai et al. published the results of a
randomized controlled trial comparing a low-calorie, low fat diet (1500 kcal for women, 1800
kcal for men, 30% total fat); a low-calorie Mediterranean diet (1500 kcal for women, 1800 kcal
for men, up to 35% total fat); and a low carbohydrate diet (20 g/day for two months with a
gradual increase to a maximum of 120 g/day, calories unrestricted). Participants on the low
carbohydrate diet and the Mediterranean diet lost significantly more weight over 2 years than
participants on the low fat diet (-4.7 kg, -4.4 kg, and -2.9 kg, respectively). Sacks et al. compared
weight loss among participants placed on four diets that varied in macronutrient content (low fat,
average protein; low fat, high protein; high fat, average protein; and high fat, high protein) and
found comparable weight loss among all groups after 2 years. The targeted percentages of energy
derived from fat, protein and carbohydrates in the four diets were: 20, 15 and 65%; 20, 25, and
55%; 40, 15, and 45%; and 40, 25 and 35%. The dietary aim was to achieve a difference of 30
percentage points between the lowest carbohydrate group (target of 35% of daily caloric intake)
and the highest carbohydrate group (target of 65% of daily caloric intake). Although the dietary
prescription for carbohydrate intake was 35%, the actual average proportion of carbohydrate
intake was 42.9% at 2 years and occurred in the high-fat, high-protein group; the highest
carbohydrate intake was 53.2% at 2 years and occurred in the low-fat, average-protein group.
While this study was included in this review it has been portrayed inaccurately as an examination
of a low carbohydrate diet.
Two meta-analyses that included 87 patients and five trials, respectively, found that diets
composed of 35% to 41.4% daily energy from carbohydrate led to an average of 6.6 kg of
6

greater weight loss in studies longer than 12 weeks, and an average of 3.3 kg of greater weight
loss at 6 months, compared with higher-carbohydrate diets (> 41.4% of daily energy from
carbohydrate); the smaller meta-analysis found comparable weight loss at a year (1 kg; P = 0.15)
(Krieger et al., 2006; Nordman et al., 2006). These studies were similar in regard to the
macronutrient content of the test diets and in regard to the prescribed calorie restriction for the
low fat diet and lack of calorie restriction for the low carbohydrate diet. However, there were
significant differences with respect to study duration, patient population, frequency of dietary
counseling sessions, and patient-reported macronutrient and calorie composition. While these
studies expand our understanding of the efficacy of low carbohydrate diets on promoting weight
loss the question of why people lose more weight on a low carbohydrate diet still remains
unclear.
One theory is related to the spontaneous reduction in food intake when removing or
limiting carbohydrate foods from the diet. Interestingly, as early as 2003 Greene et al., from
Harvard University attempted to control for this spontaneous reduction when they conducted one
of the first studies to control for calorie intake when comparing the short term effects of a low
carbohydrate diet to that of a low fat diet. Participants consumed one of three diet regimens over
12 weeks: a low fat diet (55% carbohydrate, 30% fat, and 15% protein), a low carbohydrate diet
(5% carbohydrate, 65% fat and 30% protein) with the same number of calories or a low
carbohydrate diet (5% carbohydrate, 65% fat and 30% protein) supplying an extra 300 calories
per day. The researchers found that the low fat group lost 17 pounds on average, the low
carbohydrate group eating the same number of calories lost 23 pounds, and the low carbohydrate
group eating more calories lost 20 pounds. They concluded that you can eat more calories on a
low carbohydrate diet and lose similar amounts weight.
In an effort to replicate the findings of this small trial, Harvard endocrinologists Dr. Cara
Ebbeling, and David S. Ludwig conducted a similar study. The findings were published recently
in the Journal of the American Medical Association (2012). In this study they fed 21 weightreduced subjects three different diets - a low fat diet (60% carbohydrates, 20% fat, 20% protein;
high glycemic load), a diet low in refined carbohydrates (40% carbohydrate, 40% fat, and 20%
protein; moderate glycemic load), and the Atkins low carbohydrate diet (10% carbohydrate, 60%
fat, 30% protein; low glycemic load). All three groups ate the same total number of calories. The
idea was to once again debunk the theory that if losing weight were simply a matter of eating
7

fewer calories, as supporters of a low fat diet believe, then the three groups should burn calories
at the same rate.
Interestingly, they found that an Atkins diet allowed subjects to burn more calories at
rest, giving them the least chance of regaining the weight they had lost. They also had the
greatest improvements in HDL-C of all three groups. The diet low in refined carbohydrates was a
close second, while the low fat diet was least favorable. The authors concluded that a low fat diet
would produce changes that would most likely contribute to weight regain. However, it should
be noted that the low carbohydrate also produced two potentially deleterious effects, an increase
in cortisol excretion (a hormonal marker of stress) and CRP, a marker of inflammation. In
epidemiological studies higher cortisol levels were shown to promote adiposity, insulin
resistance, and cardiovascular disease (Holt et al., 2007; Purnell et al., 2009). While this study
demonstrates that low carbohydrate diets may beneficially affect metabolism and components of
metabolic syndrome (independent of calorie content) it once again raises the question of long
term safety.
Glucose Control / Diabetes
When assessing the effects of a reduced carbohydrate intake on glucose control it is
essential to differentiate the effect of carbohydrate restriction from that of weight loss so as to
determine if the diet has a beneficial effect on glycemic control independent of weight loss. This
has been studied short term in weight stable diabetic patients where carbohydrate restriction
(40% carbohydrate) resulted in a significant decrease (8.1% to 7.3%, p < 0.05) in HbA1c
compared to a high carbohydrate (55% carbohydrate) control diet (Gannon et al., 2003). In
another study of 8 diabetic men using a randomized 5-week cross over design with a 5-week
wash out period, even larger beneficial effects on glycemic control were observed with low
carbohydrate intervention (carbohydrate 20%, protein 30% and fat 50%) compared to control
diet (carbohydrate 55%, protein 15% and fat 30%) (Gannon et al., 2004). Individuals in the low
carbohydrate diet group had lower HbA1c (7.6 % vs 9.8%), glucose levels and insulin levels as
compared to those in the high carbohydrate group despite similar weight loss with both diets.
These data demonstrate that the benefits of a low carbohydrate diet on glycemic control are
independent of weight loss and are primarily due to carbohydrate reduction.

In a recent meta-analysis of the impact of low carbohydrate diets on glucose control in

individuals with type 2 diabetes (including some insulin-requiring participants) all trials with
dietary carbohydrate restriction between 4% and 45% of daily intake published between 1980
and April 2006 were evaluated (Kirk et al., 2008). The analysis suggests that low carbohydrate
diets led to significantly greater improvements in fasting glucose (4.5% predicted decrease for
each 10% decrease in proportion of caloric intake from carbohydrates; 3.2% predicted decrease
after controlling for weight loss) and HbA1c (4.4% predicted relative decrease in HbA1c for
each 10% decrease in proportion of caloric intake from carbohydrates; however, this was no
longer significant after controlling for weight loss). The duration and diet diversity of the
included studies did not affect the results (durations ranged from 4 weeks to 26 weeks; diets
included isocaloric, weight maintenance, reduced calorie, and very low to moderate carbohydrate
restriction). Of note, trials that included a low carbohydrate induction phase led to greater initial
reductions in fasting blood glucose and HbA1c. In addition, participants of studies as short as 2
weeks showed changes in HbA1c illustrating that the low carbohydrate diet rapidly impacted
glucose control. However, the meta-analysis was limited by the inclusion of three single arm
studies and one non randomized two-arm study in the 13 studies that were analyzed.
In the dietary weight loss trials reviewed previously, participants randomized to the low
carbohydrate diet groups typically improved HbA1c to a greater extent than participants in the
low fat diet groups. Westman et al. (2008) found significantly greater improvements in HbA1c
levels, body weight, and HDL-C levels of subjects with obesity and type 2 diabetes following a
low carbohydrate diet (<20 g carbohydrate per day) with no calorie restriction compared with
those eating a calorie-restricted, low glycemic index diet (55% carbohydrate, 500 kcal/day deficit
from baseline diet). Diabetes medications were reduced or eliminated in 95.2% of participants
following the low carbohydrate diet versus 62% of low glycemic index diet participants. A
subgroup analysis of individuals with diabetes in the study by Shai et al. (2008) revealed that
after 24 months, participants with diabetes in the low carbohydrate group (maximum 120 g
carbohydrate per day) had a significant (P < 0.05) decrease in HbA1c but those in the low-fat
and Mediterranean diet groups did not (0.9% 0.8% vs 0.4% 1.3% and 0.5% 1.1%,
respectively). In comparisons among these groups, however, these changes were not statistically
different. These studies demonstrate that dietary carbohydrate reduction has greater potential for

improving glycemic control in diabetes than typical Western diets, low fat diets, and even low
glycemic index diets.
These studies also corroborate the findings of previous investigations. For example, in a
study by Nielsen et al. (2005) of obese diabetic subjects, a low carbohydrate diet (20%
carbohydrate) was associated with a significant reduction in body weight, BMI, fasting blood
glucose and HbA1c at 6 months compared to the high carbohydrate group (60% carbohydrate).
Significant decreases in insulin and hypoglycemic medication requirement also were observed in
the low carbohydrate diet group. Similar improvements in glycemic control have been reported
by Boden et al. (2005) and Samaha et al. (2003). Yancy et al. (2005) evaluated the effect of a
low carbohydrate diet (initial goal of 20 g carbohydrate per day) with no calorie restriction on
blood glucose and medication use in individuals with type 2 diabetes. After 16 weeks, the 21
individuals who completed the study demonstrated a 16% decrease in mean HbA1c and only 2
subjects requiring diabetes medication did not reduce dosage; 7 subjects discontinued their
medications entirely.
To summarize, the beneficial effect of low carbohydrate diets on glycemic control is
significantly greater when compared to a low fat diet and occurs independent of weight loss in
those studies where individuals are able to achieve and maintain adequate carbohydrate
restriction. In other studies, the effect on glycemic control is proportional to weight loss, and
comparable, if not better than that seen with a conventional low fat diet. Thus, the low
carbohydrate diet is associated with significant improvement in glycemic control and has the
potential for reduction in need for exogenous insulin or oral hypoglycemic medications.
Cardiovascular Disease
Potential favorable changes in TG and HDL-C values should be weighed against
potential unfavorable changes in LDL-C and TC values when low carbohydrate diets to induce
weight loss are considered (Nordman et al., 2006). A 2008 systematic review of randomized
controlled studies that compared low carbohydrate diets to low fat, low calorie diets found that
measurements of weight, HDL-C, TG levels and systolic blood pressure were significantly better
in groups that followed low carbohydrate diets. The authors of this review also found a higher
rate of attrition in groups with low fat diets, and concluded that "evidence from this systematic
review demonstrates that low carbohydrate, high protein diets are more effective at 6 months and
10

are as effective, if not more, as low fat diets in reducing weight and cardiovascular disease risk
up to 1 year," but they also called for more long-term studies (Hession et al., 2009).
Studies show consistently that lowering carbohydrate intake raises serum HDL-C and
decreases TGs (Mensink et al., 2003; Volek et al., 2009). However, as has also been
demonstrated the effect of low carbohydrate diets on serum LDL-C is variable (see summary
table). Short-term studies (less than 12 weeks in duration), sometimes show reductions in LDLC following the use of a low carbohydrate diet while intermediate- length trials (24 and 48 weeks
in duration), report no change in LDL-C on a low carbohydrate diet (Tay et al., 2008; Gardner et
al., 2007). The longer-term trials (96 weeks) illustrate no change in LDL-C or a decrease within
the low carbohydrate diet groups (Shai et al., 2008; Sacks et al., 2009). Furthermore, in Shai et
al.s three-arm study, LDL-C was not significantly different among any of the groups, whereas in
the study by Sacks et al. LDL-C decreased in all four arms but the greatest decrease was with the
lowest fat and highest carbohydrate diets.
Studies also have investigated the impact of low carbohydrate diets in individuals with
diabetes, hypertriglyceridemia, and atherogenic dyslipidemia. A meta-analysis in patients with
diabetes evaluated the impact of low carbohydrate diets on blood lipids after controlling for the
effect of weight loss and found that for every 10% decrease in carbohydrate intake, triglycerides
decreased by 7.6% 0.6% (P = 0.001) (Nordman et al., 2006). Stoernell et al. (2008) compared
the effects of two diets on lipids after randomizing 28 patients with hypertriglyceridemia to 8
weeks of a low carbohydrate diet (15% carbohydrate, 20-30% protein, and 55-65% fat) or a low
fat diet (50-60% carbohydrate, 15% protein, and 30% fat). Atherogenic very low-density
lipoprotein cholesterol, the predominant lipoprotein carrier of triglyceride, declined 46% in the
low carbohydrate diet group while increasing 36% in the low fat diet group (P = 0.045).
In 2009, Volek et al. compared the effects of 2 hypocaloric diets on 40 subjects with
atherogenic dyslipidemia: a low carbohydrate diet (12% CHO) and a low fat diet (56% CHO).
After 12 weeks, subjects on the low carbohydrate diet had more favorable TG (51%), HDL-C
(13%), and TC/HDL-C ratio (14%) responses. In addition, the low carbohydrate group showed
more favorable responses in alternative indicators of cardiovascular risk, including low-density
lipoprotein (LDL) particle distribution. This trial was the first to provide valuable evidence
demonstrating that lipid subfractions and the more atherogenic components of the cholesterol
lipoproteins improve to a greater extent on a low carbohydrate diet than a low fat diet.
11

In another study, Sharman et al. (2004) compared the effects of 2 calorie-restricted diets
on serum lipid levels in 15 overweight men: a low carbohydrate diet (<10% carbohydrate, 60%
fat, and 30% protein) and a low fat diet (55% carbohydrate, <30% fat, 20% protein). Subjects
were randomized to 1 of the diets for a 6-week period, after which they crossed over to the other
diet for another 6 weeks. Both diets had the same effect on total cholesterol and neither diet
changed HDL-C. LDL-C was reduced only by the low fat diet (18%), whereas the fasting
serum TG level was only reduced by the low carbohydrate diet (44%). Significant increases in
large LDL-1 particles and decreases in smaller, more atherogenic LDL-3 and LDL-4 particles
were seen only after the low carbohydrate diet was ingested.
While diets and weight loss in particular, tend to lower serum LDL-C and total
cholesterol levels, there is substantial variation. More reliable are the effects of low carbohydrate
diets on improvements in HDL-C, TG, and, most importantly, LDL particle size. The possibility
that it is not LDL-C that is atherogenic but rather the predominance of small, dense LDLs (the
so-called pattern B phenotype) is a possible factor and should be considered in future studies
evaluating the safety and efficacy of a low carbohydrate diet.
In summary, these studies further support the previous finding that low carbohydrate
diets improve dyslipidemia associated with metabolic syndrome to a greater extent than higher
carbohydrate diets or lower fat diets. In addition, most of the dietary randomized controlled trials
found that low carbohydrate diets did not, on average, adversely impact LDL-C, and they
frequently decreased it. However, due to the considerable variation in the LDL-C response to
low carbohydrate diets it is advisable to monitor individuals for LDL-C elevations.
Athletic Performance
Early studies of dietary manipulation and athletic performance demonstrate that reducing
dietary carbohydrate in the diet from a normal intake (~50%) to a diet in which less than 11% of
the total energy is contributed by carbohydrate can significantly reduce exercise time to
exhaustion during high-intensity exercise (Maughan & Poole, 1981; Greenhaff et al., 1987a, b).
In contrast, in later years, Hargreaves et al. (1997) found that muscle glycogen lowering exercise
and the consumption of diets with either high (80% carbohydrate) or low (25% carbohydrate) did
not result in differences in high-intensity exercise performance in trained male cyclists.

12

Over time similar studies of the effects of diet on the capacity to perform high-intensity
training have been conducted using trained subjects and less extreme dietary manipulations: the
majority of these failed to produce significant differences in performance (See table 2). Thus,
the evidence supporting the benefits of training with high carbohydrate availability on
performance outcomes is reliant on a small number of training studies comparing groups with
moderate ( 5g/kg/d) and high ( 10 g/kg/d) carbohydrate intakes. While these studies
provide clear evidence of superior restoration of muscle glycogen stores when athletes consume
a high carbohydrate diet only three studies have shown improvements in performance (Simonsen
et al., 1991; Achten et al., 2004; Halson et al., 2004).
Despite inconsistencies in the research, official guidelines for athletes prepared during the
1990s were unanimous in their recommendation of high carbohydrate intakes (55% - 75% of
total calories) as part of the daily training diet. This belief was based on the perceived benefit of
promoting muscle glycogen recovery on a daily basis (American Dietetic Association, 1993).
Such recommendations have been criticized over the years in large part based on the lack of
available evidence to provide clear support for the benefits of high carbohydrate intakes on
training and performance.
One plausible theory for this lack of evidence is the ability of athletes to adapt to lower
muscle glycogen stores resulting from a reduced carbohydrate intake such that there is no
impairment of training or performance outcomes. This theory underpins the recently described
train low, compete high protocol - training with low glycogen/carbohydrate availability to
enhance the training response, but competing with high fuel availability to promote performance.
It has been suggested that training in a low glycogen state and reduced carbohydrate intake may
result in greater training adaptation, such as increased oxidative capacity (Hansen et al., 2005;
Yeo et al., 2008; Mortin et al., 2009). In 2005 the Hansen study marked the first study to
demonstrate that under certain circumstances training with low muscle glycogen can be
beneficial. Unfortunately, the use of untrained subjects performing a very fixed amount of work
in each training bout made the findings difficult to apply to real life athletes.
Subsequently, Yeo et al. (2008) used a similar training model to that of Hansen but in
well trained cyclists and found that self-selected training intensity was reduced when highintensity interval training was initiated with low muscle glycogen. However, after completing the
training period, time trial cycling performance was improved to a similar extent in the high and
13

low glycogen groups. Another interesting finding was that training with low muscle glycogen
resulted in higher rates of whole-body fat oxidation during exercise, whereas training with high
muscle glycogen had no effect on substrate metabolism. Using an identical protocol to Yeo et al.
Hulston et al. (2010) also showed that power output was compromised when trained cyclists
commenced high-interval training sessions with low versus normal glycogen stores. In addition,
they reported that measures of fat oxidation during submaximal cycling were greater after low
glycogen training. Taken together, the results from these studies clearly demonstrate that,
independent of prior training status, short-term interventions in which approximately half of the
sessions are commenced with low muscle glycogen levels promote training adaptations (i.e.,
increases the activities of enzymes involved in energy metabolism and mitochondrial biogenesis,
increases rates of whole-body and muscle-derived fat oxidation) to a greater extent than when all
workouts are undertaken with normal or elevated glycogen stores. However, despite creating
conditions that should, in theory, enhance exercise capacity, the effects of this train-low strategy
on a range of performance measures still remains unclear.
It also is important to consider the potential pitfalls that may arise from the train low
strategies. As mentioned previously, there is evidence that training low reduces the ability to
train increasing the perception of effort and reducing power outputs. Most athletes aim to
achieve high power outputs and work rates in training as a preparation for competition. This is an
important consideration because the outcome-defining activities in most sports are conducted at
high intensity. The possibility that hypocaloric low carbohydrate diets may impact high intensity
performance and/or daily training performance also is of great concern. Finally, the effect of
repeated training with low carbohydrate status on the risk of illness (Gleeson et al., 2004), injury
(Brouns et al., 1986) and overtraining (Petibois et al., 2003) need to be considered. Of note is the
finding that a higher carbohydrate intake was able to reduce (but not prevent) the development of
over-reaching symptoms (fatigue, impaired performance, sleep and mood disturbance, altered
hormonal responses to stress, etc.), which can occur when a period of intensified training is
undertaken (Achten et al., 2004; Halson et al., 2004).
For recreational athletes who seek to use a modest exercise program to reduce body fat
composition the possibility of increased fat oxidation during exercise is appealing. While
evidence supports the idea that exercising in the fasted state or while consuming a carbohydraterestricted diet can increase fat oxidation, this is usually accompanied by an increase in the
14

subjective perception of effort, and the total amount of work done, and therefore the effect on
energy balance, is likely to be less (Hawley, 2011). In addition, it is possible that increase in
perceived effort associated with exercise in a carbohydrate-depleted state also is likely to
discourage some from adhering to an exercise program. Yet for others, improvements in body
weight may be motivation enough to continue.
In summary, there is insufficient evidence to provide guidelines to athletes for
incorporating train low strategies into their training programs. While there may be a sound
hypothesis that training with a reduced carbohydrate diet can amplify the training response, there
is no clear proof that this leads to performance enhancements. In addition, there are potential
disadvantages to the health and performance of the athlete, including the likelihood that training
low may interfere with the volume or intensity of training.
For most athletes both diet and exercise routines change continuously within their
training program, some training sessions are performed with low carbohydrate status (overnight
fasting, twice daily training sessions, little carbohydrate intake during the workout), while others
are undertaken using strategies that promote carbohydrate status (more recovery time, post-meal,
carbohydrate intake during the session). It makes sense that sessions undertaken at lower
intensity or at the beginning of a training cycle are most appropriate for train low strategies.
Conversely, sessions that are performed in the transition to peaking for competition are likely to
require higher intensity and may be best undertaken with greater carbohydrate availability.
Therefore the key is to find the optimal balance of nutrition strategies that achieves an athletes
overall nutrition goals, suits their lifestyle and resources, and maximizes their training and
competition performances.
Adherence
Studies of low carbohydrate diets show attrition rates that are comparable to most
conventional diets with values ranging from 0% to 50%. While adherence is difficult to assess
and largely based on self reported dietary records, in studies of low-carbohydrate diets adherence
may be evaluated through tests for ketonuria, an indicator of carbohydrate restriction. In studies
ranging from six months to two years, the percentage of participants who tested positive for
urinary ketones was greater in the low carbohydrate group than in the low-fat group, (Yancy et
al., 2004; Foster et al., 2003) conventional group (Stern et al., 2004), or Mediterranean diet group
15

(Shai et al., 2008) after two weeks, but this difference decreased progressively with time spent
following the diet (Yancy et al., 2004; Westman et al., 2002; Foster et al., 2003). Self-reported
dietary adherence also decreased with time spent following the diet (Stern et al., 2004; Westman
et al., 2002).
In the dietary weight loss trials a direct correlation is identified between dietary
adherence and weight loss regardless of the type of dietary treatment (Foster et al., 2010;
Dansinger et al., 2005; Sacks et al., 2009). The motivation to maintain restrictive dietary
patterns typically diminishes over time. The investigators of each trial concluded that a variety of
diets are successful in reducing weight and cardiac risk factors, but only for those who can
sustain a high dietary adherence level.
In the study by Dansinger et al. they compared several diets differing in percentages of
energy from carbohydrate over a 12-month period (ranging from 46% to 50% of calories a day at
baseline and returning to 40% to 48% of calories a day at 12 months). The investigators noted
that dietary adherence, as assessed by diet records and self-assessment, decreased progressively
over the one-year intervention studies in all treatment groups. They concluded that no single diet
produces satisfactory adherence rate.
In general, regardless of diet type, diminished adherence is typical after 6 months. In
trials of low-carbohydrate diets a very low incidence of urinary ketosis after 6 months is
reported, suggesting that sustaining a reduced intake of carbohydrates is often futile. These trials
confirm the longstanding success of programs such as Weight Watchers which incorporate
attendance at group sessions as a strategy for achieving weight loss goals.
When looking at other factors related to adherence, scores of satiety and hunger, as
measured by questionnaire (Layman et al., 2003) were similar in participants consuming a low
fat diet (NCEP Step 2) or a low carbohydrate diet (20% of energy as carbohydrate) for eight
weeks (Stoernell et al., 2008). In a six-month study, physical complaints and weakness were
reported more frequently among those following a low carbohydrate diet (no more than 20 g of
carbohydrate a day) than in those following a low-fat diet (no more than 30% of energy from fat)
(Yancy et al., 2004). Westman et al. (2002) reported similar adverse effects, compared with
baseline, in participants consuming no more than 25 g of carbohydrate a day for six months.

16

Timeline Summary of Significant Research

In 2003 a systematic review of low carbohydrate diets conducted by Bravata et al.
reported that weight loss is associated with only the duration of the diet and the restriction of
energy intake, not reduced carbohydrate content. Of the 2609 articles identified only 107 were
included for review. Of those, only 5 evaluated participants for more than 90 days, but these
were not randomized and had no control group. While low-carbohydrate diets had no significant
adverse effect on serum lipid, fasting serum glucose, and fasting serum insulin levels, or blood
pressure they reported that participant weight loss while using low-carbohydrate diets was
principally associated with decreased caloric intake and not with reduced carbohydrate content.
Therefore, the authors concluded that there is insufficient evidence to make recommendations for
or against the use of low-carbohydrate diets.
Later that same year three randomized trials were published reporting on the longer-term
effect of low carbohydrate diets. Samaha et al. (2003) completed a study of 132 obese subjects
comparing the efficacy of low carbohydrate and low fat diets. Subjects were randomized to
either an ad-libitum low carbohydrate diet ( 30 g carbohydrate) or an energy-restricted low fat
diet (500 kcal/day deficit, 30% fat) for 6 months. Those on the low carbohydrate diet had lost
3.9 kg more weight after 6 months, but at 12 months the difference was no longer significant.
The authors found that severely obese subjects with a high prevalence of diabetes or the
metabolic syndrome lost more weight during six months on a low carbohydrate diet than on a
calorie- and fat-restricted diet, with a relative improvement in insulin sensitivity and triglyceride
levels, even after adjustment for the amount of weight lost. However, this finding should be
interpreted with caution, given the small between-group differences in weight loss in these obese
subjects and the short duration of the study. Thus, it was concluded that future studies evaluating
long-term cardiovascular outcomes are needed before a carbohydrate-restricted diet can be
endorsed.
Brehm et al. (2003) completed a similar 6 month intervention study with 53 obese
women. Like the Samaha findings individuals in the low carbohydrate diet (maximum intake of
20 g carbohydrate per day with increase to 40-60 g) group lost significantly more weight than
those on the calorie restricted, moderately low fat diet with a macronutrient intake of 55%
carbohydrate, 15% protein, and 30% fat (8.5 kg vs 3.9 kg) after 6 months (p<0.001). The third
study by Foster et al. 2003 was conducted over one year and is considered to be the first truly
17

randomized, controlled study of the efficacy and safety of low carbohydrate diets. This trial
included 63 obese subjects that were randomly assigned either to low carbohydrate (<20 g
carbohydrate with gradual increase) or conventional low fat diets (1200 to 1500 kcal per day for
women and 1500 to 1800 kcal per day for men with approximately 60% of calories from
carbohydrate, 25% from fat and 15% from protein). After 6 months the low carbohydrate group
had better outcomes, with a weight loss of 7.0% versus 3.2% (p=0.02), but after 12 months the
difference between the groups again was no longer significant (4.4% vs 2.5%).The authors
reported that adherence was poor and attrition was high in both groups. Once again it was
concluded that larger studies of longer duration were required to determine the long-term safety
and efficacy of low carbohydrate diets.
In 2004 two more significant studies were published. Yancy et al. 2004 completed a
study of 120 overweight, hyperlipidemic subjects comparing the efficacy of low carbohydrate
(initial goal of 20 g carbohydrate per day) and low fat diets (<30% fat and deficit of 500 to
1000 kcal/d). After 6 months of treatment they concluded that when compared with a low fat
diet, a low carbohydrate diet program had better participant retention and greater weight loss.
During active weight loss, serum TG levels decreased more and HDL-C level increased more
with the low carbohydrate diet than with the low fat diet.
Stern et al. 2004 conducted a 12 month study of 132 obese adults and found that
participants on a low carbohydrate diet (< 30 g carbohydrate per day) had more favorable overall
outcomes at 1 year than did those on a conventional calorie restricted diet (<30% fat and deficit
of 500 kcal/d). While weight loss was similar between groups, the effects on atherogenic
dyslipidemia and glycemic control were more favorable with a low carbohydrate diet even after
adjustment for differences in weight loss.
By the end of 2004, Astrup et al. completed a Rapid Review of published research on the
topic of low carbohydrate diets. Acknowledging that the global rise in overweight and obesity
had intensified, the authors wanted to weigh in on the research surrounding low carbohydrate
diets. Despite the plethora of recently published research they concluded that there remains an
urgent need for longer and larger studies in obese and moderately overweight individuals.
Specifically, they encouraged studies up to 2 years in obese individuals with impaired glucosetolerance to examine the potential of low carbohydrate diets to prevent type 2 diabetes.

18

Although the authors went on to question the merits of a low carbohydrate diet they nevertheless
recommend longer-term studies to judge them more effectively.
As would be expected, in 2005 the focus shifted toward individuals with diabetes. As
previously mentioned, in a study of 28 overweight subjects with type 2 diabetes Yancy et al.
2005 found that a low carbohydrate diet (<20 g carbohydrate per day) improved glycemic control
in patients with type 2 diabetes such that diabetes medications were discontinued or reduced in
most participants. This study supported the argument that low carbohydrate diets can be at least
a partial remedy for some forms of diabetes (and may lend support to the argument that some
forms of diabetes may in fact be caused by high carbohydrate diets).
In 2006 Nielsen & Joensson also completed a study of type 2 diabetics randomly
assigned to either a low-carbohydrate diet (20% carbohydrate), or conventional highcarbohydrate diet (55-60% carbohydrate) for 22 months. All test subjects consumed the same
amount of calories. Over the first 6 months the low-carbohydrate group was found to have
significantly greater weight loss and glycemic control. In addition, the low-carbohydrate group
was found to mostly maintain their weight loss and glycemic control through the 22 months of
the study. This study suggests that while weight reduction is primarily caused by decreased
caloric intake, decreased energy efficiency also plays a role. That is, a high-starch, highcarbohydrate diet may stimulate appetite and disturb energy balance in patients with the
metabolic syndrome and type 2 diabetes. Whereas, a reduction of carbohydrates normalizes the
balance, reduces insulin concentrations and favors utilization of stored fat as fuel as well as
significantly reducing insulin resistance. They went on to conclude that weight loss in
overweight persons is improved by a higher proportion of protein, presumably due to protein's
effect on satiety and/or metabolic efficiency. This study helped pave the way to promoting a
reduction in carbohydrates for patients with type 2 diabetes even if independent of weight loss.
In 2007 Gardner et al. were the first to conduct a randomized controlled trial to show
that an Atkins (low carbohydrate diet) led to greater weight loss than a low fat diet or other
popular weight loss diet at a duration greater than 6 months. The trial included 311 overweight
women each following one of four previously described diet plans (Atkins, Zone, LEARN, and
Ornish). The authors found that premenopausal overweight and obese women assigned to follow
the Atkins diet, which had the lowest carbohydrate intake, lost more weight and experienced
more favorable overall metabolic effects at 12 months than women assigned to follow the Zone,
19

Ornish, or LEARN diets. Following this landmark study questions still remained about long-term
effects and mechanisms of a low carbohydrate, high protein, high fat diet, however its
consideration as a feasible alternative recommendation for weight loss was continuing to grow.
In July 2008, the New England Journal of Medicine published the results of the first twoyear study involving a low carbohydrate diet. The study compared a low carbohydrate diet (20
g/day for two months with a gradual increase to a maximum of 120 g/day, calories unrestricted),
a 30%-fat diet recommended by the American Heart Association, and a 35%-fat "Mediterranean"
diet that included portions of olive oil and nuts. Among the 272 participants who completed the
study, the average weight loss was about 6.3 pounds for the low-fat group, 9.7 pounds for the
Mediterranean-diet group, and 10.3 pounds for the low-carbohydrate group, and the low-fat
group showed less improvement than the other groups in blood cholesterol levels (Shai et al.,
2008). Of note, the actual average dietary fat content of the three groups turned out to be 30%
for the "low fat" group, 33% for the Mediterranean diet group and 40% for the low carbohydrate
group. The amount of weight lost was small, differences among the groups were not large, and
the study was done with close monitoring and may not reflect what happens when people diet on
their own.
Using a similar design, Sacks et al. 2009 randomly assigned 811 overweight adults to
one of four test diets varying in macronutrient distribution (low fat, average protein; low fat, high
protein; high fat, average protein; high fat, high protein) and found comparable weight loss
among all groups after 2 years. The dietary aim was to achieve a difference of 30% between the
lowest (35% of calories) and highest carbohydrate (65% of calories) groups. However, the actual
average proportion of intake was 42.9% at 2 years for the lowest carbohydrate groups. While
this amount of carbohydrate intake is not considered comparable to the other reported low
carbohydrate diets it does lend further support to the argument that low carbohydrate diets are
not sustainable long term.
In 2012 a four year study titled "Effects of Dietary Composition on Energy Expenditure
During Weight-Loss Maintenance" was released for publication. Ebbeling et al. conducted the
study at Boston Children's Hospital to examine the effects of three dieting regimens on resting
energy expenditure and total energy expenditure and other hormonal and metabolic markers. The
study closely followed 21 overweight and obese males and females aged 10-40 years, and
compared three different diets - a low fat diet (60% carbohydrates, 20% fat, 20% protein; high
20

glycemic load), a diet low in refined carbohydrates (40% carbohydrate, 40% fat, and 20%
protein; moderate glycemic load), and the Atkins low carbohydrate diet (10% carbohydrate, 60%
fat, 30% protein; low glycemic load). Reduction of the resting metabolic rate as a result of
dieting, a known factor in the failure of dieting, was the least in the very low carbohydrate diet.
In addition, measured total energy expenditure in the patients was the highest in the very low
carbohydrate diet, suggesting that a very low carbohydrate diet would be the most likely to
produce a sustained weight loss. A possible negative side effect was that CRP levels, a marker
for possible future cardiovascular disease, trended higher in the very low carbohydrate diet.

Meta Analyses
Many of these and other landmark clinical trials have been summarized in meta-analyses.
The meta-analyses mentioned in this review are limited to randomized controlled trials that
directly compare low carbohydrate diets to other diets. For example, in 2006 Nordman et al.
published the first meta-analysis of low carbohydrate trials (conducted from January 1, 1980 to
February 28, 2005) (Foster et al., 2003; Samaha et al. 2003; Dansinger et al., 2005) and found
that low carbohydrate diets were more beneficial than low fat diets for weight loss, for increasing
HDL-C, and for lowering TG at 6 months with sustained lipid improvements to 1 year but
similar weight loss. However, potential favorable changes in TG and HDL-C values should be
weighed against potential unfavorable changes in LDL-C values when low carbohydrate diets to
induce weight loss are considered (Nordman, et al. 2006).
More recently a meta-analyses of randomized controlled studies (from January 2000 to
March 2007) that compared low-carbohydrate diets to low-fat/low-calorie diets found that
measurements of weight, HDL cholesterol, triglyceride levels and systolic blood pressure were
significantly better in groups that followed low-carbohydrate diets. The authors also found a
higher rate of attrition in groups with low-fat diets. They conclude that low-carbohydrate, highprotein diets are more effective at 6 months and are as effective, if not more, as low-fat diets in
reducing weight and cardiovascular disease risk up to 1 year (Hession et al., 2009).

21

Conclusions
Given the evidence to date, even opponents of a low carbohydrate diet would agree that
following the diet for a short period of time is probably not harmful. The concerns lie in the lack
of emphasis placed on long-term changes in eating behavior, such as controlling portions or
mindful eating. There is difficulty in supporting any diet that restricts food groups and/or specific
foods. As the resulting diet can lack fiber, certain vitamins and minerals, and the thousands of
phytochemicals found in our foods that can have health-promoting benefits. In addition, most
low carbohydrate diets suggest a carbohydrate level that is well below the 130 grams/day
recommended by the Dietary Reference Intakes - values that are beleived to be optimal for
health.
A benefit of the low-carbohydrate diet, however, is that it recommends eliminating many
foods that are high in calories and low in nutritional value, such as sweetened beverages and
empty-calorie snack foods. In addition, it may have helped increase the focus on using whole
grains, fruits, and vegetables as healthy sources of carbohydrates. In general, the greatest
challenge in dieting is to figure out how to consume fewer calories - and to eat healthfully on a
regular basis. Given today's "eat more" food environment this is a much more important research
problem than whether low carbohydrate or low-fat diets work better for weight loss. Diets that
are successful in causing weight loss can emphasize a range of fat, protein, and carbohydrate
compositions yet still have beneficial effects on risk factors for cardiovascular disease and
diabetes. To be successful however, diets must be tailored to an individuals personal and
cultural preferences in order to have the greatest chance for long term success.
The past several years have produced numerous investigations into the impact of low
carbohydrate diets on weight loss, diabetes, and cardiovascular risk improvement. Repeated
studies demonstrate that low carbohydrate diets improve parameters of metabolic syndrome,
building confidence in its therapeutic potential for this disease and other obesity-related diseases.
Although our understanding of the safest, most tolerable, and most effective weight loss diet
continues to grow amid continued research, it may be that tailoring therapy to the individual is
the best therapeutic approach. The evidence to date suggests that low carbohydrate dietary
patterns should be tested in larger, multisite randomized trials with clinically meaningful
outcomes such as diabetes incidence and cardiovascular events.

22

References
1. Achten J, Halson SH, Moseley L, et al. Higher dietary carbohydrate content during
intensified running training results in better maintenance of performance and mood state. J
Appl Physiol 2004: 96: 13311340.
2. Adam-Perrot A, Clifton P, Brouns F. Low-carbohydrate diets: nutritional and physiological
aspects. Obes Rev. 2006;7:49-58.
3. American Dietetic Association. Position stand of the American Dietetic Association and the
Canadian Dietetic Association: nutrition for physical fitness and athletic performance for
adults. J Am Diet Assoc 1993: 93: 691696.
4. Arora, S.K. & McFarlane, S.I. (2005) The case for low carbohydrate diets in diabetes
management. Nutr. Metab. (Lond.) 2, 16.
5. Astrup A, Meinert Larsen T, Harper A. Atkins and other low-carbohydrate diets: hoax or an
effective tool for weight loss? Lancet. 2004 Sep 4-10;364(9437):897-9.
6. Astrup, A. Macronutrient balances and obesity: the role of diet and physical activity. Public
Health Nutr. (1999) 2, 341347.
7. Aude, Y.W., Agatston, A.S., Lopez-Jimenez, F. et al. The National Cholesterol Education
Program diet vs a diet lower in carbohydrates and higher in protein and monounsaturated fat:
a randomized trial. Arch. Intern. Med. (2004) 164, 21412146.
8. Ben-Avraham S, Harman-Boehm I, Schwarz - fuchs D, et al. Dietary strategies for patients
with type 2 diabetes in the era of multi-approaches: review and results from the Dietary
Intervention Randomized Controlled Trial (DIRECT). Diabetes Res Clin Pract 2009; 86
(suppl 1):S41S48.
9. Boden G, Sargrad K, Homkko C, et al. Effect of a low-carbohydrate diet on appetite, blood
glucose levels, and insulin resistance in obese patients with type 2 diabetes. Ann Intern Med
2005; 142: 403411.
10. Bradley U, Spence M, Courtney CH, et al. Low-fat versus low-carbohydrate weight
reduction diets: effects on weight loss, insulin resistance, and cardiovascular risk a
randomized control trial. Diabetes 2009; 58: 27412748.
11. Bravata DM, Sanders L, Huang J, et al. Efficacy and safety of low-carbohydrate diets: a
systematic review. JAMA. 2003;289:1837-1850.
12. Brehm BJ, Seeley RJ, Daniels SR, DAlessio DA. A randomized trial comparing a very low
carbohydrate diet and a calorie-restricted low fat diet on bodyweight and cardiovascular risk
factors in healthy women. J Clin Endocrinol Metab 2003;88:1617-23.
13. Brehm BJ, Spang SE, Lattin BL, et al. The role of energy expenditure in the differential
weight loss in obese women on low-fat and low-carbohydrate diets. J Clin Endocrinol Metab
2005; 90: 14751482.
14. Brinkworth GD, Buckley JD, Noakes M, et al. Long-term effects of a very low-carbohydrate
diet and a low-fat diet on mood and cognitive function. Arch Intern Med 2009;169: 1873
1880.
15. Brinkworth GD, Noakes M, Buckley JD, et al. Long-term effects of a very-low-carbohydrate
weight loss diet compared with an isocaloric low-fat diet after 12 months. Am J Clin Nutr
2009; 90: 2332.
16. Brinkworth GD, Noakes M, Clifton PM, et al. Comparative effects of very low-carbohydrate,
high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal shortchain fatty acids and bacterial populations. Br J Nutr 2009; 101: 14931502.
23

17. Brouns F, Saris WHM, Ten Hoor F. Nutrition as a factor in the prevention of injuries in
recreational and competitive downhill skiing. J Sports Med 1986: 26: 8591.
18. Burke LM, Kiens B, Ivy JL. Carbohydrates and fat for training and recovery. J Sports Sci
2004: 22: 1530.
19. Costill DL, Flynn MG, Kirwan JP, et al. Effects of repeated days of intensified training on
muscle glycogen and swimming performance. Med Sci Sports Exerc 1988: 20: 249254.
20. Cox GR, Clark SA, Cox AJ, et al. Daily training with high carbohydrate availability
increases exogenous carbohydrate oxidation during endurance cycling. J Appl Physiol 2010:
109: 126134.
21. Daly ME, Paisey R, Millward BA, et al. Short-term effects of severe dietary carbohydraterestriction advice in Type 2 diabetes--a randomized controlled trial. Diabet Med. 2006
Jan;23(1):15-20.
22. Dansinger ML, Gleason JA, Griffith JL, et al. Comparison of the Atkins, Ornish, Weight
Watchers, and Zone diets for weight loss and heart disease risk reduction: a randomized trial.
JAMA 2005;293:43-53.
23. Das SK, Gilhooly CH, Golden JK, et al. Long-term effects of 2 energy-restricted diets
differing in glycemic load on dietary adherence, body composition, and metabolism in
CALERIE: a 1-y randomized controlled trial. Am J Clin Nutr 2007;85:1023-30.
24. Davis NJ, Tomuta N, Schechter C, et al: Comparative study of the effects of a 1-year dietary
intervention of a low-carbohydrate diet versus a low-fat diet on weight and glycemic control
in type 2 diabetes. Diabetes Care. 2009; 32: 11471152.
25. Due A, Toubro S, Skov AR, Astrup A. Effect of normal-fat diets, either medium or high in
protein, on body weight in overweight subjects: a randomised 1-year trial. Int J Obes Relat
Metab Disord 2004;28: 1283-90.
26. Dyson PA, Beatty S, Matthews DR. A low-carbohydrate diet is more effective in reducing
body weight than healthy eating in both diabetic and non-diabetic subjects. Diabet Med. 2007
Dec;24(12):1430-5. Epub 2007 Oct 29.
27. Dyson PA: A review of low and reduced carbohydrate diets and weight loss in type 2
diabetes. J Hum Nutr Diet 2008; 21: 530 538.
28. Ebbeling CB, Swain JF, Feldman HA, et al. Effects of dietary composition on energy
expenditure during weight-loss maintenance. JAMA. 2012 Jun 27;307(24):2627-34.
29. Esposito K, Maiorino MI, Ciotola M, et al. Effects of a Mediterranean-style diet on the need
for antihyperglycemic drug therapy in patients with newly diagnosed type 2 diabetes: a
randomized trial. Ann Intern Med. 2009 Sep 1;151(5):306-14.
30. Farnsworth E, Luscombe ND, Noakes M, et al. Effect of a high-protein, energy-restricted
diet on body composition, glycemic control, and lipid concentrations in overweight and
obese hyperinsulinemic men and women. Am J Clin Nutr 2003; 78: 3139.
31. Foster GD, Wyatt HR, Hill JO, et al. A randomized trial of a low-carbohydrate diet for
obesity. N Engl J Med 2003;348: 2082-90.
32. Foster, G.D., Wyatt, H.R., Hill, J.O. et al. Weight and metabolic outcomes after 2 years on a
low-carbohydrate versus low-fat diet. Ann. Intern. Med. (2010) 153, 147157.
33. Gannon MC, Hoover H, Nuttall FQ. Further decrease in glycated hemoglobin following
ingestion of a LoBAG30 diet for 10 weeks compared to 5 weeks in people with untreated
type 2 diabetes. Nutr Metab (Lond). 2010 Jul 29;7:64.

24

34. Gannon MC, Nuttall FQ, Saeed A, Jordan K, Hoover H. An increase in dietary protein
improves the blood glucose response in persons with type 2 diabetes. Am J Clin Nutr. 2003
Oct;78(4):734-41.
35. Gannon MC, Nuttall FQ: Effect of a high protein, low-carbohydrate diet on blood glucose
control in people with type 2 diabetes. Diabetes 2004; 53: 23752382.
36. Gardner CD, Kiazand A, Alhassan S, et al. Comparison of the Atkins, Zone, Ornish, and
LEARN diets for change in weight and related risk factors among overweight premenopausal
womenthe A to Z Weight Loss Study: a randomized trial. JAMA. 2007;297:969-977.
37. Gleeson M, Nieman DC, Pedersen BK. Exercise, nutrition and immune function. J Sports Sci
2004: 22: 115122.
38. Greenhaf PL, Gleeson M, Maughan RJ (1987a) The effects of dietary manipulation on blood
acid-base status and the performance of high intensity exercise. Eur J Appl Physiol 56:331337
39. Greenhaf PL, Gleeson M, Whiting PH, Maughan RJ (1987b) Dietary composition and acidbase status: limiting factors in the performance of maximal exercise in man? Eur J Appl
Physiol 56:444-450
40. Halson SH, Lancaster GI, Achten J, et al. Effects of carbohydrate supplementation on
performance and carbohydrate oxidation after intensified cycling training. J Appl Physiol
2004: 97: 12451253.
41. Hansen AK, Fischer CP, Plomgaard P, et al. Skeletal muscle adaptation: training twice every
second day vs. training once daily. J Appl Physiol 2005: 98: 9399.
42. Hargreaves M, Finn JP, Withers RT, et al. Effect of muscle glycogen availability on
maximal exercise performance. Eur J Appl Physiol 1997;75:188-192
43. Hawley JA, Tipton KD, Millard-Stafford ML. Promoting training adaptations through
nutritional interventions. J Sports Sci 2006: 24: 709721.
44. Hawley JA. Fat adaptation science: low-carbohydrate, high- fat diets to alter fuel utilization
and promote training adaptation. Nestle Nutr Inst Workshop Ser. 2011;69:59-71; discussion
71-7.
45. Hession M, Rolland C, Kulkarni U, et al: Systematic review of randomized controlled trials
of low-carbohydrate vs. low-fat/low-calorie diets in the management of obesity and its
comorbidities. Obes Rev 2009; 10: 3650.
46. Holt HB, Wild SH, Wareham N, et al. Differential effects of fatness, fitness and physical
activity energy expenditure on whole-body, liver and fat insulin sensitivity. Diabetologia.
2007 Aug;50(8):1698-706.
47. Hulston CJ, Venables MC, Mann CH, et al. Training with low muscle glycogen enhances fat
metabolism in well-trained cyclists. Med Sci Sports Exerc 2010; March 25.
48. Johnston CS, Tjinn SL, Swann PD, et al: Ketogenic low-carbohydrate diets have no
metabolic advantage over nonketogenic low-carbohydrate diets. Am J Clin Nutr 2006; 83:
10551061.
49. Kerstetter JE, O'brien KO, Caseria DM, et al. The impact of dietary protein on calcium
absorption and kinetic measures of bone turnover in women. J Clin Endocrinol Metab 2005;
90: 2631.
50. Kirk E, Reeds DN, Finck BN, et al: Dietary fat and carbohydrates differentially alter insulin
sensitivity during caloric restriction. Gastroenterology 2009; 136: 1552 1560.
51. Kirk JK, Graves DE, Craven TE, et al.: Restricted-carbohydrate diets in patients with type 2
diabetes: a meta-analysis.J Am Diet Assoc 2008, 108:91100.
25

52. Kirwan JP, Costill DL, Mitchell JB, et al. Carbohydrate balance in competitive runners
during successive days of intense training. J Appl Physiol 1988: 65: 26012606.
53. Krieger JW, Sitren HS, Daniels MJ, Langkamp-Henken B: Effects of variation in protein and
carbohydrate intake on body mass and composition during energy restriction: a metaregression 1. Am J Clin Nutr 2006, 83:260274.
54. Lamb DR, Rinehardt KF, Bartels RL, et al. Dietary carbohydrate and intensity of interval
swim training. Am J Clin Nutr 1990: 52: 10581063.
55. Layman DK, Boileau RA, Erickson DJ, et al. A reduced ratio of dietary carbohydrate to
protein improves body composition and blood lipid profiles during weight loss in adult
women. J Nutr 2003; 133: 411417.
56. LeCheminant JD, Gibson CA, Sullivan DK, et al. Comparison of a low carbohydrate and low
fat diet for weight maintenance in overweight or obese adults enrolled in a clinical weight
management program. Nutr J 2007;6:36.
57. Maughan RJ, Poole DC (1981) The effects of glycogen-loading regimen on the capacity to
perform anaerobic exercise. Eur J Appl Physiol 46:211-219
58. McLaughlin T, Carter S, Lamendola C, et al. Effects of moderate variations in macronutrient
composition on weight loss and reduction in cardiovascular disease risk in obese, insulinresistant adults. Am J Clin Nutr 2006;84:813-21.
59. McMillan-Price J, Petocz P, Atkinson F, et al. Comparison of 4 diets of varying glycemic
load on weight loss and cardiovascular risk reduction in overweight and obese young adults:
a randomized controlled trial. Arch Intern Med 2006;166: 1466-75.
60. Meckling KA, OSullivan C, Saari D. Comparison of a low-fat diet to a low-carbohydrate
diet on weight loss, body composition, and risk factors for diabetes and cardiovascular
disease in free-living, overweight men and women. J Clin Endocrinol Metab. 2004;89:27172723.
61. Mensink RP, Zock PL, Kester AD, Katan MB: Effects ofdietary fatty acids and
carbohydrates on the ratio of serumtotal to HDL cholesterol and on serum lipids and
apolipoproteins: a meta-analysis of 60 controlled trials. Am J Clin Nutr2003, 77:11461155.
62. Morton JP, Croft L, Bartlett JD, et al. Reduced carbohydrate availability does not modulate
training-induced heat shock protein adaptations but does upregulate oxidative enzyme
activity in human skeletal muscle. J Appl Physiol 2009: 106: 15131521.
63. Muzio F, Mondazzi L, Harris W, et al: Effects of moderate variations in the macronutrient
content of the diet on cardiovascular disease risk factors in obese patientswith the metabolic
syndrome. Am J Clin Nutr 2007; 86: 946951.
64. Nielsen JV, Joensson E. Low-carbohydrate diet in type 2 diabetes. Stable improvement of
bodyweight and glycemic control during 22 months follow-up. Nutr Metab (Lond). 2006 Jun
14;3:22.
65. Nielsen JV, Jnsson E, Nilsson AK. Lasting improvement of hyperglycaemia and
bodyweight: low-carbohydrate diet in type 2 diabetes--a brief report. Ups J Med Sci.
2005;110(1):69-73.
66. Noakes M, Keough JB, Foster PR, Clifton PM. Effect of an energy-restricted, high-protein,
low-fat diet relative to a conventional low-fat, high-carbohydrate diet on weight loss, body
composition, nutritional status, and markers of cardiovascular health in obese women. Am J
Clin Nutr 2005;81:1298-306.

26

67. Nordmann AJ, Nordmann A, Briel M, et al.: Effects of low-carbohydrate vs low-fat diets on
weight loss and cardiovascular risk factors: a meta-analysis of randomized controlled trials.
Arch Intern Med 2006, 166:285293.
68. Parker B, Noakes M, Luscombe N, Clifton P. Effect of a high-protein, high-monounsaturated
fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes Care.
2002 Mar;25(3):425-30.
69. Petibois C, Cazorla G, Poortmans JR, Dlris G. Biochemical aspects of overtraining in
endurance sports: the metabolism alteration process syndrome. Sports Med 2003: 33: 8394.
70. Phinney SD, Bistrian BR, Evans WJ, et al. The human metabolic response to chronic ketosis
without caloric restriction: preservation of submaximal exercise capability with reduced
carbohydrate oxidation. Metabolism 1983; 32: 769776.
71. Purnell JQ, Kahn SE, Samuels MH, et al. Enhanced cortisol production rates, free cortisol, and
11beta-HSD-1 expression correlate with visceral fat and insulin resistance in men: effect of weight
loss. Am J Physiol Endocrinol Metab. 2009 Feb;296(2):E351-7. Epub 2008 Dec 2.

72. Reddy ST, Wang CY, Sakhaee K, Brinkley L, Pak CY. Effect of low-carbohydrate highprotein diets on acid-base balance, stone-forming propensity, and calcium metabolism. Am J
Kidney Dis 2002; 40: 265274.
73. Sacks FM, Bray GA, Carey VJ, et al.: Comparison of weight-loss diets with different
compositions of fat, protein, and carbohydrates. N Engl J Med 2009, 360:859873.
74. Samaha FF, Iqbal N, Seshadri P, et al. A low-carbohydrate as compared with a low-fat diet in
severe obesity. N Engl J Med 2003;348:2074-81.
75. Shai I, Schwarzfuchs D, Henkin Y, et al. Weight loss with a low-carbohydrate,
Mediterranean, or low-fat diet. N Engl J Med 2008;359:229-41.
76. Sharman MJ, Gmez AL, Kraemer WJ, Volek JS. Very low-carbohydrate and low-fat diets
affect fasting lipids and postprandial lipemia differently in overweight men. J Nutr. 2004(a)
Apr;134(4):880-5.
77. Sharman MJ, Volek JS. Weight loss leads to reductions in inflammatory biomarkers after a
very-low-carbohydrate diet and a low-fat diet in overweight men. Clin Sci (Lond) 2004(b);
107: 365369.
78. Sheard NF, Clark NG, Brand-Miller JC, et al: Dietary carbohydrate (amount and type) in the
prevention and management of diabetes: a statement by the American Diabetes Association.
Diabetes Care 2004; 27:22662271.
79. Sherman WM, Doyle J, Lamb DR, Strauss RH. Dietary carbohydrate, muscle glycogen, and
exercise performance during 7 d of training. Am J Clin Nutr 1993: 57: 2731.
80. Simonsen JC, Sherman WM, Lamb DR, et al.. Dietary carbohydrate, muscle glycogen, and
power output during rowing training. J Appl Physiol 1991: 70: 15001505.
81. Stern L, Iqbal N, Seshadri P, et al. The effects of low-carbohydrate versus conventional
weight loss diets in severely obese adults: one-year follow-up of a randomized trial. Ann
Intern Med 2004;140: 778-85.
82. Stoernell CK, Tangney CC, Rockway SW: Short-term changes in lipoprotein subclasses and
C-reactive protein levels of hypertriglyceridemic adults on low-carbohydrate and low-fat
diets. Nutr Res 2008, 28:443449.
83. Tay J, Brinkworth GD, Noakes M, et al. Metabolic effects of weight loss on a very-lowcarbohydrate diet compared with an isocaloric high-carbohydrate diet in abdominally obese
subjects. J Am Coll Cardiol. 2008;51:59-67.
84. Vogt M, Puntschart A, Howald H, et al. Effects of dietary fat on muscle substrates,
metabolism, and performance in athletes. Med Sci Sports Exerc 2003: 35: 952960.
27

85. Volek JS, Phinney SD, Forsythe CE, et al.: Carbohydrate restriction has a more favorable
impact on the metabolic syndrome than a low fat diet. Lipids 2009, 44:297309.
86. Volek JS, Sharman MJ, Gmez AL, et al: Comparison of a very low-carbohydrate and lowfat diet on fasting lipids, LDL subclasses, insulin resistance, and postprandial lipemic
responses in overweight women. J Am Coll Nutr 2004; 23: 177184.
87. Volek JS, Westman EC. Very low-carbohydrate weight-loss diets revisited. Cleve Clin J Med
2002;69:849, 853, 856-858.
88. Westman EC, Feinman RD, Mavropoulos JC, et al.: Low carbohydrate nutrition and
metabolism. Am J Clin Nutr 2007, 86:276284.
89. Westman EC, Mavropoulos J, Yancy WS, Volek JS: A review of low-carbohydrate
ketogenic diets. Curr Atheroscler Rep 2003, 5:476483.
90. Westman EC, Yancy WS Jr, Mavropoulos JC, et al.: The effect of a low-carbohydrate,
ketogenic diet versus a low glycemic index diet on glycemic control in type 2 diabetes
mellitus. Nutr Metab (Lond) 2008, 5:36.
91. Westman EC, Yancy WS, Edman JS, Tomlin KF, Perkins CE. Effect of 6-month adherence
to a very low carbohydrate diet program. Am J Med. 2002 Jul;113(1):30-6.
92. Wolever TM, Gibbs AL, Mehling C, et al: The Canadian Trial of Carbohydrates in Diabetes
(CCD), a 1-y controlled trial of low-glycemic index dietary carbohydrate in type 2 diabetes:
no effect on glycated hemoglobin but reduction in C-reactive protein. Am J Clin Nutr 2008;
87: 114125.
93. Yancy WS Jr, Almirall D, Maciejewski ML, et al.: Effects of two weight-loss diets on healthrelated quality of life. Qual Life Res 2009, 18:281289.
94. Yancy WS Jr, Foy M, Chalecki AM, Vernon MC, Westman EC. A low-carbohydrate,
ketogenic diet to treat type 2 diabetes. Nutr Metab (Lond). 2005 Dec 1;2:34.
95. Yancy WS Jr, Olsen MK, Dudley T, Westman EC: Acid-base analysis of individuals
following two weight loss diets. Eur J Clin Nutr 2007, 61:14161422.
96. Yancy WS Jr, Olsen MK, Guyton JR, Bakst RP, Westman EC. A low-carbohydrate
ketogenic diet versus a low-fat diet to treat obesity and hyperlipidemia: a randomized,
controlled trial. Ann Intern Med 2004;140:769-77.
97. Yeo WK, Paton CD, Garnham AP, Burke LM, Carey AL, Hawley JA. Skeletal muscle
adaptation and performance responses to once a day versus twice every second day
endurance training regimens. J Appl Physiol 2008: 105 (5): 14621470.

28