A Randomized Trial of a Low-Carbohydrate Diet for Obesity
Gary D. Foster, Ph.D., Holly R. Wyatt, M.D., James O. Hill, Ph.D., Brian G. McGuckin, Ed.M., Carrie Brill, B.S., B. Selma Mohammed, M.D., Ph.D., Philippe O. Szapary, M.D., Daniel J. Rader, M.D., Joel S. Edman, D.Sc., and Samuel Klein, M.D.
Background Despite the popularity of the low-carbohydrate, high-protein,high-fat (Atkins) diet, no randomized, controlled trials haveevaluated its efficacy.
Methods We conducted a one-year, multicenter, controlled trialinvolving 63 obese men and women who were randomly assignedto either a low-carbohydrate, high-protein, high-fat diet ora low-calorie, high-carbohydrate, low-fat (conventional) diet.Professional contact was minimal to replicate the approach usedby most dieters.
Results Subjects on the low-carbohydrate diet had lost moreweight than subjects on the conventional diet at 3 months (mean[±SD], –6.8±5.0 vs. –2.7±3.7percent of body weight; P=0.001) and 6 months (–7.0±6.5vs. –3.2±5.6 percent of body weight, P=0.02), butthe difference at 12 months was not significant (–4.4±6.7vs. –2.5±6.3 percent of body weight, P=0.26). Afterthree months, no significant differences were found betweenthe groups in total or low-density lipoprotein cholesterol concentrations.The increase in high-density lipoprotein cholesterol concentrationsand the decrease in triglyceride concentrations were greateramong subjects on the low-carbohydrate diet than among thoseon the conventional diet throughout most of the study. Bothdiets significantly decreased diastolic blood pressure and theinsulin response to an oral glucose load.
Conclusions The low-carbohydrate diet produced a greater weightloss (absolute difference, approximately 4 percent) than didthe conventional diet for the first six months, but the differenceswere not significant at one year. The low-carbohydrate dietwas associated with a greater improvement in some risk factorsfor coronary heart disease. Adherence was poor and attritionwas high in both groups. Longer and larger studies are requiredto determine the long-term safety and efficacy of low-carbohydrate,high-protein, high-fat diets.
At any given time, approximately 45 percent of women and 30percent of men in the United States are trying to lose weight.1Despite these efforts, the prevalence of obesity has doubledin the past 20 years2 and has become a major public health problem.3The conventional dietary approach to weight management, recommendedby the leading research and medical societies,4,5,6,7 is a high-carbohydrate,low-fat, energy-deficit diet. Low-carbohydrate, high-protein,high-fat diets have become increasingly popular, and many best-sellingdiet books have promoted this approach.8,9 The Atkins diet,originally published in 1973 and again in 1992 and 2002, maybe the most popular of these diets. More than 10 million copiesof Atkins's diet book have been sold,10 and four times as manydieters have read one of the Atkins books as have read any otherdiet book.11
Despite its longevity and popularity, no randomized trials evaluatingthe efficacy of the Atkins diet have been published.12,13 Datafrom short-term, uncontrolled studies indicate that the Atkinsdiet induces weight losses of 8.3 percent after 8 weeks14 and10.3 percent after 24 weeks.15
We conducted a one-year, multicenter, randomized, controlledtrial to evaluate the effect of the low-carbohydrate, high-protein,high-fat Atkins diet on weight loss and risk factors for coronaryheart disease in obese persons. The subjects were randomly assignedto follow either a low-carbohydrate, high-protein, high-fatAtkins diet or a high-carbohydrate, low-fat, energy-deficitconventional diet. Professional contact was minimal, so as toapproximate the approach used by most dieters.
Methods
Subjects
A total of 63 persons (43 women and 20 men) participated inthe study (Table 1). All subjects completed a comprehensivemedical examination and routine blood tests. Potential subjectswere excluded if they had clinically significant illnesses,including type 2 diabetes; were taking lipid-lowering medications;were pregnant or lactating; or were taking medications thataffect body weight. All subjects provided written informed consent,and the protocol was approved by the institutional review boardsof the participating institutions.
Table 1. Base-Line Characteristics of the Subjects.
Study Design
The subjects were randomly assigned at each site, with use ofa random-number generator, to follow either the low-carbohydratediet or the conventional diet. Subjects in both groups wereinstructed to take a daily multivitamin supplement and met witha registered dietitian for 15 to 30 minutes at 3, 6, and 12months to review dietary issues.
Low-Carbohydrate Diet
The 33 subjects who were assigned to the low-carbohydrate, high-protein,high-fat diet met individually with a registered dietitian beforebeginning the program to review the central features of thediet (available as Supplementary Appendix 1 with the full textof this article at http://www.nejm.org), which involves limitingcarbohydrate intake without restricting consumption of fat andprotein. For the first two weeks, carbohydrate intake is limitedto 20 g per day and is then gradually increased until a stableand desired weight is achieved. Each subject was given a copyof Dr. Atkins' New Diet Revolution,10 which details the Atkinsdiet program. Subjects were instructed to read the book andfollow the diet as described.
Conventional Diet
The 30 subjects who were assigned to the conventional diet alsomet with a registered dietitian before beginning the programto review the components of a high-carbohydrate, low-fat, low-caloriediet (1200 to 1500 kcal per day for women and 1500 to 1800 kcalper day for men, with approximately 60 percent of calories fromcarbohydrate, 25 percent from fat, and 15 percent from protein)and to receive instructions about calorie counting. Subjectswere given a copy of The LEARN Program for Weight Management,17which provides 16 lessons covering various aspects of weightcontrol. The nutritional information in the manual was consistentwith the dietary recommendations provided by the study dietitianand with the Department of Agriculture Food Guide Pyramid.18Subjects were instructed to read the manual and follow the programas described.
Outcomes
Body weight was measured with the use of calibrated scales (Detecto6800, Cardinal) while the subjects were wearing light clothingand no shoes at base line and at weeks 2, 4, 8, 12, 16, 20,26, 34, 42, and 52. Blood pressure and urinary ketones werealso assessed at base line and at weeks 2, 4, 8, 12, 16, 20,26, 34, 42, and 52. Blood samples were obtained after subjectsfasted overnight at base line and at 3, 6, and 12 months todetermine serum lipoprotein concentrations. An oral glucose-tolerancetest was performed at base line and at 3, 6, and 12 months.After subjects fasted overnight, blood samples were obtainedfor the measurement of plasma glucose and insulin concentrationsbefore and 30, 60, 90, and 120 minutes after the oral administrationof a 75-g glucose load. In addition, insulin sensitivity, basedon fasting plasma glucose and insulin concentrations, was assessedwith the use of quantitative insulin-sensitivity check index16:1 ÷ [(log fasting serum insulin level, in microunitsper milliliter) + (log fasting glucose level, in milligramsper deciliter)].
Analyses of Samples
Serum total cholesterol, high-density lipoprotein (HDL) cholesterol,and triglyceride concentrations were assayed according to proceduresrecommended by the Centers for Disease Control and Preventionand the National Heart, Lung, and Blood Institute.19 The low-densitylipoprotein (LDL) cholesterol concentration was calculated accordingto the Friedewald formula20 in all but one subject, who hada triglyceride concentration greater than 400 mg per deciliter(4.52 mmol per liter). Plasma insulin was measured by radioimmunoassay,and plasma glucose by a glucose oxidase autoanalyzer (YellowSprings Instruments). The area under the curve (AUC) for theplasma glucose concentration and for the insulin concentrationwas calculated.21 Urinary ketone concentrations were measuredwith dipsticks (Ketostix 2880, Bayer) and characterized dichotomouslyas negative (0 mg per deciliter) or positive (5 to 100 mg perdeciliter).
Statistical Analysis
Analysis of variance revealed no effects of the research siteon weight loss or attrition at 3, 6, or 12 months, so the dataon all the subjects were analyzed together. A t-test for independentsamples was used to assess differences in base-line variablesbetween the groups. Two sets of analyses were conducted. Theprimary analysis was a repeated-measures analysis of variancein which the base-line value was carried forward in the caseof missing data. In a secondary analysis, an analysis of covariance(in which initial weights were covariates) was used to examinechanges in weight from base line to the end of the study, forthose who completed the study, or at the time of the last follow-upvisit, for those who did not complete the study. A chi-squareanalysis was performed to determine differences between groupsin categorical variables, and correlations with categoricalvariables were assessed with Spearman's rho coefficient. Triglyceridevalues were not normally distributed, so the log-transformedvalues were analyzed. Results are presented as percent changesto facilitate clinical interpretation, although all analysesinvolved absolute values and were conducted with the use ofSPSS software (version 11.0).22
Results
Weight
In the analysis in which base-line values were carried forwardin the case of missing values, the group on the low-carbohydratediet had lost significantly more weight than the group on theconventional diet at 3 months (P=0.001) and 6 months (P=0.02),but the difference in weight loss was not statistically significantat 12 months (P=0.26) (Table 2 and Figure 1A).
Table 2. Percent Changes in Weight, Blood Pressure, Serum Lipoprotein Concentrations, and Oral Glucose Tolerance in an Analysis in Which Base-Line Values Were Carried Forward in the Case of Missing Data.
Figure 1. Mean (±SE) Percent Change in Weight among Subjects on the Low-Carbohydrate Diet and Those on the Conventional (Low-Calorie, High-Carbohydrate) Diet, According to an Analysis in Which Base-Line Values Were Carried Forward in the Case of Missing Values (Panel A) or an Analysis That Included Data on Subjects Who Completed the Study and Data Obtained at the Time of the Last Follow-up Visit for Those Who Did Not Complete the Study (Panel B).
In Panel B, the low-carbohydrate group had 28 subjects at 3 months, 24 subjects at 6 months, and 20 subjects at 12 months and the conventional-diet group had 21 subjects at 3 months, 18 subjects at 6 months, and 17 subjects at 12 months. Asterisks indicate a significant difference (P<0.05) between the groups.
Attrition
A total of 49 subjects completed 3 months of the study (28 onthe low-carbohydrate diet and 21 on the conventional diet),42 subjects completed 6 months (24 on the low-carbohydrate dietand 18 on the conventional diet), and 37 subjects completed12 months (20 on the low-carbohydrate diet and 17 on the conventionaldiet). The percentage of subjects who had dropped out of thestudy at 3, 6, and 12 months was higher in the group followingthe conventional diet (30, 40, and 43 percent, respectively)than in the group following the low-carbohydrate diet (15, 27,and 39 percent, respectively), but these differences were notstatistically significant. Overall, 59 percent of subjects completedthe study, and 88 percent of those who completed the six-monthassessment completed the full study. When the analysis includeddata on subjects who completed the study and data obtained atthe time of the last follow-up visit for those who did not completethe study, the pattern of weight loss was similar to that obtainedwhen the base-line values were carried forward in the case ofmissing data. Subjects on the low-carbohydrate diet lost significantlymore weight than the subjects on the conventional diet at 3months (P=0.002) and 6 months (P=0.03), but the difference inweight loss was not statistically significant at 12 months (P=0.27)(Table 3 and Figure 1B).
Table 3. Percent Changes in Weight, Blood Pressure, Serum Lipoproteins, and Oral Glucose Tolerance in an Analysis That Included Data on Subjects Who Completed the Study and Data Obtained at the Time of the Last Follow-up Visit for Those Who Did Not Complete the Study.
Urinary Ketones
During the first three months, the percentage of patients whotested positive for urinary ketones was significantly greaterin the group on the low-carbohydrate diet than in the groupon the conventional diet (Figure 2), but there were no significantdifferences between the groups after three months. There wasno significant relation between weight loss and ketosis at anytime during the study.
Figure 2. Percentage of Subjects with a Positive Urinary Ketone Concentration, According to Whether They Were on the Low-Carbohydrate Diet or the Conventional (Low-Calorie, High-Carbohydrate) Diet.
A positive urinary ketone concentration was defined as 5 to 100 mg per deciliter. Asterisks indicate a significant difference (P<0.003) between the groups.
Blood Pressure
Systolic blood pressure did not change significantly in eithergroup during the study (Table 2 and Table 3). Diastolic pressuredecreased in both groups, but there were no significant differencesbetween groups.
Oral Glucose-Tolerance Test
The area under the glucose curve did not change significantlyin either group throughout the study. The area under the insulincurve decreased in both groups, but there were no significantdifferences between groups (Table 2 and Table 3). There wereno significant differences between groups in insulin sensitivity(assessed by the quantitative insulin-sensitivity check index16)throughout the study period. Both groups had significant increasesin insulin sensitivity at six months, but the values were notsignificantly different from base line at one year (Table 2and Table 3).
Serum Lipoproteins
The effects of the diets on serum lipoproteins are shown inTable 2 and Table 3 and Figure 3. There were no significantdifferences between groups in the total or LDL cholesterol concentration,except at month 3, when values were significantly lower in thegroup on the conventional diet than in the group on the low-carbohydratediet. In contrast, the relative increase in HDL cholesterolconcentrations and the relative decrease in triglyceride concentrationswere greater in the group on the low-carbohydrate diet thanin the group on the conventional diet throughout most of thestudy. The results of the analyses that included data on subjectswho completed the study and data obtained at the time of thelast follow-up visit for those who did not complete the study(Table 3) were nearly identical to the analyses in which base-linevalues were carried forward in the case of missing data (Table 2)with respect to blood pressure, insulin sensitivity, andserum lipoproteins.
Figure 3. Mean (±SE) Percent Change in Serum Concentrations of Triglycerides (Panel A), Total Cholesterol (Panel B), Low-Density Lipoprotein (LDL) Cholesterol (Panel C), and High-Density Lipoprotein (HDL) Cholesterol (Panel D) among Subjects on the Low-Carbohydrate Diet and Those on the Conventional (Low-Calorie, High-Carbohydrate) Diet.
Data were obtained at the end of the study for subjects who completed the study and at the time of the last follow-up visit for those who did not complete the study. The low-carbohydrate group had 28 subjects at 3 months, 24 subjects at 6 months, and 20 subjects at 12 months. The conventional-diet group had 21 subjects at 3 months, 18 subjects at 6 months, and 17 subjects at 12 months. Asterisks indicate a significant difference (P<0.05) between the groups.
Discussion
The results of this multicenter, randomized, controlled trialdemonstrate that the low-carbohydrate, high-protein, high-fatAtkins diet produces greater weight loss (an absolute differenceof approximately 4 percent) than a conventional high-carbohydrate,low-fat diet for up to six months, but that the differencesdo not persist at one year. The magnitude of weight loss atsix months in the low-carbohydrate group approximates that achievedby standard behavioral23 and pharmacologic24 treatments. Theseweight losses are particularly noteworthy because the diet wasimplemented in a self-help format and subjects had little contactwith health professionals. The lack of a statistically significantdifference between the groups at one year is most likely dueto greater weight regain in the low-carbohydrate group and thesmall sample size. These data suggest that long-term adherenceto the low-carbohydrate Atkins diet may be difficult.
The difference in weight loss between the two groups in thefirst six months demonstrates an overall greater energy deficitin the low-carbohydrate group, despite unrestricted proteinand fat intake in this group and instructions to restrict energyintake in the conventional-diet group. When the energy contentof an energy-deficit diet is stable, macronutrient compositiondoes not influence weight loss.25,26,27,28 The mechanism responsiblefor the decreased energy intake induced by a low-carbohydratediet with unrestricted protein and fat intake is not known butmay be related to the monotony or simplicity of the diet, alterationsin plasma or central satiety factors, or other factors thataffect appetite and dietary adherence. Our data suggest thatketosis was unlikely to be responsible for the increased weightloss with the low-carbohydrate diet, since we did not find anyrelation between the presence of urinary ketones and weightloss. Furthermore, urinary ketones were not present in mostsubjects on either diet after the first six months.
Although subjects with diabetes were excluded from our study,many — if not most — of our subjects, because oftheir obesity, were probably insulin-resistant with respectto glucose metabolism.29 Treatment with either diet was associatedwith an improvement in insulin sensitivity as determined byan oral glucose-tolerance test; progressively less insulin wassecreted to maintain the same blood glucose concentrations.These data do not demonstrate an effect of macronutrient composition,independent of weight loss, on insulin sensitivity in obesesubjects without diabetes. However, the results of these metabolicstudies should be interpreted with caution, given the study'srelatively small sample size and the one-year duration. Additionalstudies in which more precise measures of insulin sensitivityare used are needed to evaluate this issue more carefully.
An important health concern of consuming unrestricted amountsof saturated fat is the potential to increase the LDL cholesterolconcentration, which is an established risk factor for coronaryheart disease. In fact, at three months, the LDL cholesterolconcentration tended to increase in the subjects on the low-carbohydratediet but decreased in the subjects on the conventional diet,so the difference between groups was significant. Over the longterm, however, the LDL cholesterol concentration among subjectson the low-carbohydrate diet was similar to base-line values,and the changes in LDL cholesterol concentrations did not differsignificantly between the groups. These data suggest that theincreased weight loss associated with the low-carbohydrate dietmay offset the adverse effect of saturated fat intake on serumLDL cholesterol concentrations. Nonetheless, weight loss withthe low-carbohydrate diet was not associated with the decreasesin LDL cholesterol usually observed with moderate weight loss.4,30
In contrast, the low-carbohydrate diet was associated with greaterdecreases in serum triglycerides and greater increases in HDLcholesterol than was the conventional diet, and the levels ofboth are also important risk factors for coronary heart disease.31,32,33The magnitude of these changes approximates that obtained withpharmacologic treatments, such as derivatives of fibric acidand niacin.31 Although part of this benefit may be due to thegreater weight loss with the low-carbohydrate diet, the changesare greater than those expected from a moderate weight lossalone.30 Therefore, it is likely that the macronutrient compositionof the diet contributed to the improvement in the HDL cholesterol–triglycerideaxis. High-carbohydrate, low-fat diets decrease HDL cholesterolconcentrations and increase serum triglyceride concentrations,34,35,36,37whereas low-carbohydrate, high-fat diets decrease triglycerideconcentrations16,27,37 and increase HDL cholesterol concentrations.15Moreover, replacing dietary polyunsaturated or monounsaturatedfat with carbohydrate is associated with an increased risk ofcoronary heart disease, as predicted by changes in triglycerideand HDL cholesterol concentrations.38
The overall effect of the low-carbohydrate diet in comparisonwith a conventional diet on the risk of coronary heart diseasein our subjects is uncertain. As compared with the conventionaldiet, the low-carbohydrate diet was associated with a greaterimprovement in some risk factors for coronary heart disease(serum triglycerides and serum HDL cholesterol), but not others(blood pressure, insulin sensitivity, and serum LDL cholesterol).Moreover, the clinical significance of the favorable changesin the HDL cholesterol–triglyceride axis in the settingof a high fat intake is not clear. Additional, long-term studiesare needed to determine whether increased serum HDL cholesterolconcentrations and decreased serum triglyceride concentrationshave the same effect on cardiovascular outcomes when one isconsuming a diet high in saturated fat. It is also possiblethat the large amount of saturated fats and small amounts offruits, vegetables, and fiber consumed during the low-carbohydratediet can independently increase the risk of coronary heart disease.39,40Therefore, at the present time, there is not enough informationto determine whether the beneficial effects of the Atkins dietoutweigh its potential adverse effects on the risk of coronaryheart disease in obese persons.
Our study has several limitations. The self-help nature of treatment,which is consistent with the way in which the low-carbohydratediet is typically used, probably contributed to the attritionrate of 41 percent. This high rate of attrition underscoresthe difficulty of long-term compliance with either diet, whendiet therapy is given with minimal supervision. More comprehensivebehavioral treatment (e.g., weekly group meetings or self-monitoring)would probably have decreased attrition, increased adherence,and made possible a comparison with clinic-based treatmentsfor obesity.23 Our study was focused on weight and specificrisk factors for coronary heart disease. We did not evaluatethe effect of the low-carbohydrate diet on other important clinicalend points, such as renal function, bone health, cardiovascularfunction, and exercise tolerance. Finally, our findings shouldnot be generalized to overweight subjects or to obese subjectswith serious obesity-related diseases, such as diabetes andhypercholesterolemia. Additional studies are needed in thesepopulations to evaluate the safety and efficacy of low-carbohydrate,high-protein, high-fat diets.
Supported by grants from the National Institutes of Health (RR00036,RR00040, RR00051, AT1103, DK 37948, DK 56341, DK48520, DK42549,DK02703, and AT00058).
Dr. Foster reports having received consulting fees from AbbottLaboratories and HealtheTech and lecture fees from Abbott Laboratoriesand Roche Laboratories. Dr. Wyatt reports having received consultingfees from Ortho-McNeil, USANA, and GlaxoSmithKline and lecturefees from Roche Laboratories, Abbott Laboratories, Slim-Fast,and Ortho-McNeil. Dr. Hill reports having received consultingfees from HealtheTech, Johnson & Johnson, Procter &Gamble, Coca-Cola, and the International Life Sciences Institute;lecture fees from Abbott Laboratories, Roche Laboratories, andKraft Foods; and grant support from M&M Mars, Procter &Gamble, and Abbott Laboratories. Dr. Szapary reports havingreceived lecture fees from AstraZeneca and Kos Pharmaceuticalsand grant support from AstraZeneca. Dr. Klein reports havingreceived consulting fees from Roche Laboratories and HealtheTech,lecture fees from Ortho-McNeil, and grants from GlaxoSmithKlineand Regeneron.
Source Information
From the University of Pennsylvania School of Medicine, Philadelphia (G.D.F., B.G.M., P.O.S., D.J.R.); University of Colorado Health Sciences Center, Denver (H.R.W., J.O.H., C.B.); Washington University School of Medicine, St. Louis (B.S.M., S.K.); and Thomas Jefferson University, Philadelphia (J.S.E.).
Address reprint requests to Dr. Foster at the University of Pennsylvania, 3535 Market St., Suite 3027, Philadelphia, PA 19104-3309, or at fosterg{at}mail.med.upenn.edu.
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Low-Carbohydrate Diets as Compared with Low-Fat Diets
Duggirala M. K., Mundell W. C., Mikkilineni P., Aziz I., Garrido J. A., Roberts C. K., Barnard R. J., Samaha F. F., Stern L., Iqbal N., Foster G. D., Hill J. O., Klein S.
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Correspondence
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