A Low-Carbohydrate as Compared with a Low-Fat Diet in Severe Obesity
Frederick F. Samaha, M.D., Nayyar Iqbal, M.D., Prakash Seshadri, M.D., Kathryn L. Chicano, C.R.N.P., Denise A. Daily, R.D., Joyce McGrory, C.R.N.P., Terrence Williams, B.S., Monica Williams, B.S., Edward J. Gracely, Ph.D., and Linda Stern, M.D.
Background The effects of a carbohydrate-restricted diet onweight loss and risk factors for atherosclerosis have been incompletelyassessed.
Methods We randomly assigned 132 severely obese subjects (including77 blacks and 23 women) with a mean body-mass index of 43 anda high prevalence of diabetes (39 percent) or the metabolicsyndrome (43 percent) to a carbohydrate-restricted (low-carbohydrate)diet or a calorie- and fat-restricted (low-fat) diet.
Results Seventy-nine subjects completed the six-month study.An analysis including all subjects, with the last observationcarried forward for those who dropped out, showed that subjectson the low-carbohydrate diet lost more weight than those onthe low-fat diet (mean [±SD], –5.8±8.6 kgvs. –1.9±4.2 kg; P=0.002) and had greater decreasesin triglyceride levels (mean, –20±43 percent vs.–4±31 percent; P=0.001), irrespective of the useor nonuse of hypoglycemic or lipid-lowering medications. Insulinsensitivity, measured only in subjects without diabetes, alsoimproved more among subjects on the low-carbohydrate diet (6±9percent vs. –3±8 percent, P=0.01). The amount ofweight lost (P<0.001) and assignment to the low-carbohydratediet (P=0.01) were independent predictors of improvement intriglyceride levels and insulin sensitivity.
Conclusions Severely obese subjects with a high prevalence ofdiabetes or the metabolic syndrome lost more weight during sixmonths on a carbohydrate-restricted diet than on a calorie-and fat-restricted diet, with a relative improvement in insulinsensitivity and triglyceride levels, even after adjustment forthe amount of weight lost. This finding should be interpretedwith caution, given the small magnitude of overall and between-groupdifferences in weight loss in these markedly obese subjectsand the short duration of the study. Future studies evaluatinglong-term cardiovascular outcomes are needed before a carbohydrate-restricteddiet can be endorsed.
The differences in health benefits between a carbohydrate-restricteddiet and a calorie- and fat-restricted diet are of considerablepublic interest. However, there is concern that a carbohydrate-restricteddiet will adversely affect serum lipid concentrations.1 Previousstudies demonstrating that healthy volunteers following a low-carbohydratediet can lose weight have involved few subjects, and few useda comparison group that followed consensus guidelines for weightloss.2,3 The reported effects of a carbohydrate-restricted dieton risk factors for atherosclerosis have varied.2,3,4 We performeda study designed to test the hypothesis that severely obesesubjects with a high prevalence of diabetes or the metabolicsyndrome would have a greater weight loss, without detrimentaleffects on risk factors for atherosclerosis, while on a carbohydrate-restricted(low-carbohydrate) diet than on a calorie- and fat-restricted(low-fat) diet.
Methods
Subjects
The study was approved by the institutional review board atthe Philadelphia Veterans Affairs Medical Center, and an approvedconsent form was signed by each subject. Inclusion criteriawere an age of at least 18 years and a body-mass index (theweight in kilograms divided by the square of the height in meters)of at least 35. Exclusion criteria were a serum creatinine levelof more than 1.5 mg per deciliter (132.6 µmol per liter);hepatic disease; severe, life-limiting medical illness; inabilityof diabetic subjects to monitor their own glucose levels; activeparticipation in a dietary program; or use of weight-loss medications.During an enrollment period that lasted from May to November2001, 132 subjects from the Philadelphia Veterans Affairs MedicalCenter were randomly assigned to either the low-carbohydratediet or the low-fat diet, with use of a preestablished algorithmgenerated from a random set of numbers. We used stratified randomization,with blocking within strata, to ensure that each group wouldcontain approximately equal numbers of women, subjects withdiabetes, and severely obese subjects (body-mass index, 40 orhigher). The study was not blinded.
Study Design
The two diet groups attended separate two-hour group-teachingsessions each week for four weeks, followed by monthly one-hoursessions for five additional months; all sessions were led byexperts in nutritional counseling. Subjects received a diet-overviewhandout, instructional nutrition labels, sample menus and recipes,and a book on counting calories and carbohydrates.5 No specificexercise program was recommended. The subjects assigned to thelow-carbohydrate diet were instructed to restrict carbohydrateintake to 30 g per day or less.6 No instruction on restrictingtotal fat intake was provided. Vegetables and fruits with highratios of fiber to carbohydrate were recommended.6 The subjectsassigned to the low-fat diet received instruction in accordancewith the obesity-management guidelines of the National Heart,Lung, and Blood Institute,7 including caloric restriction sufficientto create a deficit of 500 calories per day, with 30 percentor less of total calories derived from fat.
Data Collection
The subjects' weights were measured monthly on a single calibratedscale (SRScales, SR Instruments). Other data collected at enrollmentand at six months included waist size, self-reported medicalhistory, blood pressure, and glucose and serum lipid levels,measured in blood specimens obtained after an overnight fast(Synchron LX20 Clinical Chemistry System, Beckman Coulter).Low-density lipoprotein cholesterol levels were calculated accordingto the Friedewald formula.8 Serum insulin levels were measuredby radioimmunoassay (Laboratory Corporation of America). Insulinsensitivity was estimated with use of the quantitative insulin-sensitivitycheck index as follows: 1 ÷ [(log fasting insulin level,in microunits per milliliter) + (log fasting glucose level,in milligrams per deciliter)]; this index has a good correlationwith the results of glucose-clamp studies in obese subjectsand subjects with diabetes.9 Dietary compliance was estimatedby means of a previously validated10 instrument in which subjectsare interviewed to obtain data on 24-hour recall of dietaryconsumption. Data were analyzed with Nutribase Management software(CyberSoft).
Statistical Analysis
The primary end point was weight loss at six months. Assuminga two-sided type I error of 5 percent, we estimated that wewould need 100 subjects (50 per group) for the study to have80 percent power to demonstrate a mean (±SD) weight lossthat was 5±12 kg greater in the low-carbohydrate groupthan in the low-fat group.11 Given an anticipated dropout rateof 25 percent, we set the enrollment target at 135 subjects.By six months, 79 subjects remained in the study (36 in thelow-fat group and 43 in the low-carbohydrate group). The primaryanalysis included all 132 subjects: the 79 subjects who completedthe study, the 29 subjects who dropped out but had six-monthdata available from records of routine office visits, and the24 subjects for whom the weight recorded at the last follow-upvisit was carried forward. Since the 29 subjects whose finalweight was obtained from office records were weighed on a differentscale from that used in the study, we performed a second analysisthat included all subjects, with base-line weights carried forwardfor all 53 subjects who dropped out.
For analyses of changes in dietary intake, serum lipid levels,glycemic control, and insulin sensitivity, we included all subjects,with base-line values carried forward for subjects who droppedout of the study. No interim analyses were performed.
For comparison of continuous variables between the two groups,we calculated the change from base line to six months in eachsubject and compared the mean changes in the two diet groupsusing an unpaired t-test.12 We assessed the normality of thedistribution of all variables before using the t-test. Triglyceride,insulin, and glucose levels were skewed and were therefore log-transformedfor analysis. Dichotomous variables were compared by chi-squareanalysis.12 Linear regression and two-way analysis of covariancemodels were used to correct for potentially confounding variablesand to identify interactions between variables and diet-groupassignment.12 Missing waist sizes were imputed by linear extrapolationon the basis of height and weight. All P values were two-sided,and a P value of 0.05 or less was considered to indicate statisticalsignificance. Analyses were performed with use of SPSS software(version 10.0).
Results
Base-Line Characteristics
Sixty-eight subjects were randomly assigned to the low-fat dietand 64 to the low-carbohydrate diet (Figure 1). Subjects inthe two groups were well matched with regard to base-line characteristics(Table 1). The subjects were severely obese at base line (Table 1),with a high prevalence of diabetes (39 percent) or the metabolicsyndrome without diabetes (43 percent), as previously defined.13
Figure 1. Mean (±SE) Decrease in Weight between Subjects on the Low-Carbohydrate Diet and Those on the Low-Fat Diet.
Weights for each time point include all 132 subjects. The number of subjects at each point for whom weights were either extracted from records or carried forward from a previous visit are given in parentheses. The standard errors have not been adjusted for these imputed values.
Table 1. Base-Line Characteristics of the Subjects.
Attrition
The cumulative percentage of subjects who dropped out of thestudy by months 1, 3, and 6 were 38, 44, and 47 percent, respectively,in the low-fat group and 25, 27, and 33 percent, respectively,in the low-carbohydrate group. Differences in attrition betweengroups were statistically significant by the third month (P=0.03)but were not significant at six months (P=0.10). There wereno significant differences between the groups in the characteristicsof the subjects who dropped out of the study (Table 2). Subjectson the low-carbohydrate diet attended more dietary counselingsessions than did the subjects on the low-fat diet (mean, 5.7±2.7vs. 4.3±2.7; P=0.006).
Table 2. Comparison of Base-Line Characteristics between Subjects Who Completed the Study and Those Who Dropped Out of the Study.
Assessment of Dietary Intake
After six months of dietary counseling, subjects on the low-fatdiet reported a decrease in caloric consumption while theirmacronutrient composition was close to the guidelines of theNational Heart, Lung, and Blood Institute (Table 3).7 As comparedwith the subjects on the low-fat diet, subjects on the low-carbohydratediet reported a nonsignificantly greater reduction in caloricintake (P=0.33), a significantly greater decrease in the percentageof calories from carbohydrates (P<0.001), and a significantlygreater increase in the percentage of calories from protein(P<0.001) and fat (P=0.004).
Table 3. Change from Base Line in the Composition of the Two Diets at Six Months.
Weight Loss
Subjects on the low-carbohydrate diet lost more weight during the six-month study than did those on the low-fat diet(mean,–5.8±8.6 kg vs. –1.9±4.2 kg; 95 percentconfidence interval for the difference in weight loss betweengroups, –1.6 to –6.3; P=0.002) (Figure 1). The differencein weight loss between the groups remained significant afteradjustment for base-line variables alone (age, race or ethnicgroup, sex, base-line body-mass index, base-line caloric intake,and the presence or absence of hypertension, diabetes, activesmoking, and sleep apnea) (P=0.002) and for base-line variablesplus the number of dietary counseling sessions attended (P=0.01).
A second analysis in which we carried forward the base-lineweights of subjects who dropped out of the study (i.e., assumedno weight loss in these subjects) still demonstrated greaterweight loss in the low-carbohydrate group than in the low-fatgroup (mean, –5.7±8.6 kg vs. –1.8±3.9kg; 95 percent confidence interval for the difference in weightloss between groups, –1.6 to –6.2; P=0.002).
As a measure of substantial weight loss, we found that a weightloss of at least 10 percent of the base-line weight occurredin 9 of 64 subjects on the low-carbohydrate diet (14 percent),as compared with 2 of 68 subjects on the low-fat diet (3 percent)(P=0.02). White subjects lost more weight than black subjects(mean, –13±19 kg vs. –5±12 kg; P=0.009),regardless of the diet-group assignment. There were no othersignificant differences in weight loss between the groups.
Serum Lipids
During the six-month study, there was a greater decrease inthe mean triglyceride level in the low-carbohydrate group thanin the low-fat group (–20±43 percent vs. –4±31percent, P=0.001) (Table 4). This difference remained significantafter adjustment for base-line variables (P<0.001). Subjectson the low-carbohydrate diet also had a greater mean decreasein triglyceride levels whether or not they were taking lipid-loweringdrugs (–25±38 percent vs. –8±35 percentwith lipid-lowering drugs, P=0.01; and –16±46 percentvs. –1±25 percent without lipid-lowering drugs;P=0.04). Triglyceride levels may also be affected by medicationstaken for diabetes. However, in a separate analysis of subjectswho were not taking either diabetes medications or lipid-loweringmedications (28 on the low-fat diet and 24 on the low-carbohydratediet), we still observed a greater reduction in the mean triglyceridelevel among subjects on the low-carbohydrate diet (–20±42percent vs. 2±28 percent, P=0.001). In a model adjustedfor the amount of weight lost and the base-line variables, assignmentto the low-carbohydrate diet (P=0.01) and the amount of weightlost (P<0.001) were each independent predictors of a decreasein the triglyceride level. However, comparison of subjects withinweight-loss strata demonstrated that this finding was limitedto subjects who lost more than 5 percent of their base-lineweight.
Table 4. Changes from Base Line in Serum Lipid, Glucose, Glycosylated Hemoglobin, and Uric Acid Levels at Six Months.
Black subjects had a smaller decrease in triglyceride levelsthan did white subjects (mean, –1±30 percent vs.–21±36 percent), independent of the diet-groupassignment (P=0.002), but not after adjustment for base-linevariables and the amount of weight lost (P=0.09).
The mean fasting glucose level decreased more in the low-carbohydrategroup than in the low-fat group at six months (–9±19percent vs. –2±17 percent, P=0.02) (Table 4). Thisdifference remained significant after adjustment for base-linevariables (P=0.004). However, the greater reduction in serumglucose levels in the low-carbohydrate group was limited todiabetic subjects, with no significant change in the levelsin nondiabetic subjects on either diet (Table 4). Assignmentto the low-carbohydrate diet was no longer a significant predictorof a decrease in glucose levels after adjustment for the amountof weight lost (P=0.12). There was a trend toward a greaterdecrease in mean glycosylated hemoglobin values in diabeticsubjects on the low-carbohydrate diet, as compared with thoseon the low-fat diet (P=0.06) (Table 4). By six months, sevensubjects in the low-carbohydrate group had had dose reductionsin oral hypoglycemic agents or insulin. In comparison, one subjectin the low-fat group had a dose reduction in insulin and onesubject began oral therapy.
Insulin sensitivity was measured only in subjects without diabetes.Among these subjects, those on the low-carbohydrate diet hada greater increase in insulin sensitivity than those on thelow-fat diet (6±9 percent vs. –3±8 percent,P=0.01). This difference remained significant after adjustmentfor base-line variables (P=0.001). In a model adjusted for theamount of weight lost and base-line variables, assignment tothe low-carbohydrate diet (P=0.01) and the amount of weightlost (P<0.001) were each independent predictors of an improvementin insulin sensitivity. Comparison of subjects within weight-lossstrata demonstrated a uniformly, but nonsignificantly, greaterimprovement in insulin sensitivity among those on the low-carbohydratediet within each stratum.
Blood Pressure
We did not observe significant overall or between-group changes in blood pressure.Systolic and diastolic blood pressure decreasedby 2 mm Hg and 1 mm Hg, respectively, in the low-carbohydrategroup. In the low-fat group, both systolic and diastolic bloodpressure decreased by 2 mm Hg (P=0.85 for between-group differencesin the change in systolic blood pressure and P=0.70 for between-groupdifferences in the change in diastolic blood pressure). Althoughmany subjects were receiving antihypertensive therapy at baseline (Table 1), none had a change in this therapy during thestudy.
Adverse Reactions
One subject on the low-carbohydrate diet was hospitalized withchest pain, which was ultimately determined to be unrelatedto myocardial ischemia. One subject on the low-carbohydratediet died from complications of hyperosmolar coma, which wasthought to be due to poor compliance with drug therapy for diabetes.There was no clinically significant change in the uric acidlevel in either group (Table 4).
Discussion
We found that severely obese subjects with a high prevalenceof diabetes and the metabolic syndrome lost more weight in asix-month period on a carbohydrate-restricted diet than on afat- and calorie-restricted diet. The greater weight loss inthe low-carbohydrate group suggests a greater reduction in overallcaloric intake, rather than a direct effect of macronutrientcomposition. However, the explanation for this difference isnot clear. Subjects in this group may have experienced greatersatiety on a diet with liberal proportions of protein and fat.However, other potential explanations include the simplicityof the diet and improved compliance related to the novelty ofthe diet.
Subjects in the low-carbohydrate group had greater decreasesin triglyceride levels than did subjects in the low-fat group;nondiabetic subjects on the low-carbohydrate diet had greaterincreases in insulin sensitivity, and subjects with diabeteson this diet had a greater improvement in glycemic control.No adverse effects on other serum lipid levels were observed.Most studies suggest that lowering triglyceride levels has anoverall cardiovascular benefit.14,15,16 Insulin resistance promotessuch atherosclerotic processes as inflammation,17 decreasedsize of low-density lipoprotein particles,18 and endothelialdysfunction.19 Impaired glycemic control in subjects with otherfeatures of the metabolic syndrome markedly increases the riskof coronary artery disease.20 As expected, we found that theamount of weight lost had a significant effect on the degreeof improvement in these metabolic factors. However, even afteradjustment for the differences in weight loss between the groups,assignment to the low-carbohydrate diet predicted greater improvementsin triglyceride levels and insulin sensitivity. Subjects wholost more than 5 percent of their base-line weight on a carbohydrate-restricteddiet had greater decreases in triglyceride levels than thosewho lost a similar amount of weight while following a calorie-and fat-restricted diet.
There was a consistent trend across weight-loss strata towarda greater increase in insulin sensitivity in the low-carbohydrategroup, although these changes were small and were not significantwithin each stratum. Although greater weight loss could notentirely account for the greater decrease in triglyceride levelsand increase in insulin sensitivity in the low-carbohydrategroup, we cannot definitively conclude that carbohydrate restrictionalone accounted for this independent effect. Other uncontrolledvariables, such as the types of carbohydrates selected (e.g.,the proportion of complex carbohydrates or the ratio of carbohydrateto fiber), or other unknown variables may have contributed tothis effect. In addition, more precise measurements of insulinsensitivity than we used would be needed to confirm this effectof a carbohydrate-restricted diet.
Many of our subjects were taking lipid-lowering medicationsand hypoglycemic agents. Although enrolling these subjects introducedconfounding variables, it allowed the inclusion of subjectswith the obesity-related medical disorders typically encounteredin clinical practice. Analyses from which these subjects wereexcluded still revealed greater improvements in insulin sensitivityand triglyceride levels on a carbohydrate-restricted diet thanon a fat- and calorie-restricted diet.
Our study included a high proportion of black subjects, a grouppreviously underrepresented in lifestyle-modification studies.As compared with the white subjects, the black subjects hada smaller overall weight loss. Future studies should explorewhether greater weight loss in this population can be achievedby more effective incorporation of culturally sensitive dietarycounseling.
The high dropout rate in our study occurred very early and affectedour findings. The very early dropout of these subjects may indicatethat attrition most closely reflected base-line motivation tolose weight, rather than a response to the dietary interventionitself.
Supported by funding from the Veterans Affairs Healthcare NetworkCompetitive Pilot Project Grant.
We are indebted to Drs. Michael Grippi and Stephen E. Kimmelfor their detailed review of and comments on the manuscript.
Source Information
From the Philadelphia Veterans Affairs Medical Center (F.F.S., N.I., K.L.C., D.A.D., J.M., T.W., M.W., L.S.); the Department of Medicine, Division of Cardiology (F.F.S.), and the Department of Medicine, Division of Endocrinology (N.I., P.S.), University of Pennsylvania Medical Center; and the Department of Family, Community, and Preventive Medicine, Drexel University College of Medicine (E.J.G.) — all in Philadelphia.
Address reprint requests to Dr. Samaha at Cardiology 8th Fl., MC 111C, University and Woodland Ave., Philadelphia, PA 19104, or at rick.samaha{at}med.va.gov.
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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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N Engl J Med 2003;
349:1000-1002, Sep 4, 2003.
Correspondence
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