Original Article
The Effects on Plasma Lipoproteins of a Prudent Weight-Reducing Diet, with or without Exercise, in Overweight Men and Women
N Engl J Med 1991; 325:461-466August 15, 1991
- Abstract
- Abstract
Background.
The National Cholesterol Education Program (NCEP) recommends a low-saturated-fat, low-cholesterol diet, with weight loss if indicated, to correct elevated plasma cholesterol levels. Weight loss accomplished by simple caloric restriction or increased exercise typically increases the level of high-density lipoprotein (HDL) cholesterol. Little is known about the effects on plasma lipoproteins of a hypocaloric NCEP diet with or without exercise in overweight people.
Methods.
We tested the hypothesis that exercise (walking or jogging) will increase HDL cholesterol levels in moderately overweight, sedentary people who adopt a hypocaloric NCEP diet. We randomly assigned 132 men and 132 women 25 to 49 years old to one of three groups: control, hypocaloric NCEP diet, or hypocaloric NCEP diet with exercise. One hundred nineteen of the men and 112 of the women returned for testing after one year.
Results.
After one year, the subjects in both intervention groups had reached or closely approached NCEP Step 1 dietary goals and reduced their mean body fat significantly (range of reduction in mean fat weight, 4.0 to 7.8 kg). Weight loss on the NCEP diet alone did not significantly change HDL cholesterol levels in either the men or the women as compared with the subjects in the control group. Plasma levels of HDL cholesterol increased significantly more in the men who exercised and dieted (mean [±SE] change, +13±3 percent) than in the men who only dieted (+2±3 percent, P<0.01 ) or the men who acted as controls (-4±2 percent, P<0.001). HDL cholesterol levels remained about the same in the women who exercised and dieted (+1±2 percent); they were higher than in the women who only dieted (—10±3 percent, P<0.01), but not higher than in the controls (—3±3 percent).
Conclusions.
Regular exercise in overweight men and women enhances the improvement in plasma lipoprotein levels that results from the adoption of a low-saturated-fat, low-cholesterol diet. (N Engl J Med 1991; 325:461–6.)
Media in This Article
Figure 1
Changes in Lipoprotein and Apolipoprotein Ratios in the Study Groups after One Year.Figure 2
Percent Changes in Plasma Triglyceride and Lipoprotein Cholesterol Concentrations in the Study Groups after One Year.Article Activity
- Article
SUSTAINED weight loss in moderately overweight men, whether induced by caloric restriction (with no change in dietary composition) without increased physical activity, or by increased physical activity without dietary change, results in an increase in plasma concentrations of high-density lipoprotein (HDL) cholesterol.1 The inverse relation between adiposity and HDL cholesterol levels may underlie some of the increased risk of coronary heart disease observed with obesity in men2 and women.3
In the current climate of increased attention to dietary treatment of elevated plasma levels of low-density lipoprotein (LDL) cholesterol,4 it is likely that the dietary modifications recommended to overweight people will combine caloric restriction with decreases in the intake of saturated fats and cholesterol. It is recognized that such dietary changes can reduce HDL cholesterol levels,5 and since a low HDL cholesterol level is associated with an increase in the risk of coronary heart disease, there is concern that this may partially offset the anticipated salutary effect of reducing LDL cholesterol levels.6
In a one-year controlled clinical trial in moderately overweight men and women, we examined the effects on plasma concentrations of HDL cholesterol and other lipoproteins, body composition, and blood pressure of a diet low in cholesterol and fat (particularly saturated fat), with a concomitantly lowered caloric intake, with or without a program of supervised physical activity. We hypothesized from our earlier results1 that the addition of exercise would increase the loss of body fat, improve lipoprotein levels, and reduce the estimated risk of coronary heart disease.
Methods
Experimental Design
To obtain a sample of moderately overweight people (120 to 150 percent of "ideal" body weight7), we invited men with a body-mass index (the weight in kilograms divided by the square of the height in meters) of 28 to 34 and premenopausal women with a body-mass index of 24 to 30 who were 25 to 49 years old to be screened (after having given informed consent). The subjects had to be nonsmokers, sedentary (exercising not more than twice a week and for less than 30 minutes per time), reportedly consuming on average fewer than four alcoholic drinks per day, in generally good health, and not taking medications known to affect blood pressure or lipid metabolism. Women were excluded if they had been pregnant, lactating, or taking oral contraceptives in the previous six months or if they were planning a pregnancy in the subsequent two years. Subjects were eligible if their blood pressure at rest was below 160/95 mm Hg, their plasma total cholesterol concentration was below 6.72 mmol per liter (260 mg per deciliter), and their plasma triglyceride level was below 5.65 mmol per liter (500 mg per deciliter).
Eligible persons were enrolled in three cohorts of approximately 44 men and 44 women each. After base-line evaluation, the subjects in each cohort were randomly assigned according to sex to one of three groups: diet only (a prudent diet with concomitant caloric reduction and no change in exercise level), diet plus exercise (a dietary intervention identical to that of the diet-only group, combined with increased physical activity), and control (no change in diet or exercise).
Dietary recommendations were presented by registered dietitians; they approximated the goals of the National Cholesterol Education Program (NCEP) Step 1 diet4 — i.e., approximately 55 percent of total energy was from carbohydrate and 30 percent from fat, with saturated fat reduced to 10 percent or lower and dietary cholesterol below 300 mg per day. Group sessions for the men and women together were conducted weekly for the first three months, every other week for the next three months, and monthly thereafter, with the diet-only subjects segregated from the diet-plus-exercise subjects.
The subjects in the diet-plus-exercise group were supervised in a program of aerobic exercise (primarily brisk walking and jogging) that met three days a week. They were instructed to work continuously at 60 to 80 percent of the maximal heart rate for at least 25 minutes initially, and to increase this gradually to at least 45 minutes by the fourth month of the study. The subjects maintained monthly activity logs specifying the frequency and duration or distance of walking or jogging.
Control subjects were instructed to maintain their usual diet and exercise patterns.
At base line and after one year, all the subjects completed tests for various physical measures (weight, body composition, regional adiposity, heart rate at rest, and blood pressure), aerobic fitness, dietary composition, and plasma concentrations of triglycerides, lipoprotein cholesterol, and apolipoproteins while fasting.
Clinic Procedures
Weight and height were measured with the subjects in light clothing without shoes on a standard beam balance. Body density was calculated as the mean of two determinations (separate visits) by hydrostatic weighing, with compensation for residual lung volume as measured by nitrogen dilution; relative body fat was computed according to the equation of Siri.8 Abdominal girth, measured horizontally at the umbilicus, and hip girth, measured at the largest horizontal circumference around the buttocks, were measured in the standing position (without clothing) in triplicate during two separate visits.
During two separate visits, resting systolic and diastolic blood pressure was also determined before all other procedures, after the subject had been seated quietly for at least five minutes, as previously described.9
Oxygen uptake during a graded maximal treadmill test was determined each minute with a semiautomated metabolic-analysis system, as previously described.10 Aerobic capacity (maximal oxygen uptake in milliliters of oxygen consumed per kilogram of body weight per minute) was defined as the peak value measured during the last two minutes of exercise.
Venous blood was collected in the morning, after the subjects had abstained from all food and drink except water for 12 to 16 hours and from vigorous activity for at least 12 hours. It was immediately mixed with 1.5 mg of EDTA per milliliter and kept at 4°C until centrifugation, within 30 minutes. Plasma for lipid and lipoprotein analyses was stored at 4°C until assayed within 48 hours. Samples for apolipoprotein analysis were quick-frozen on dry ice, flushed with nitrogen gas before sealing, and stored at —80°C until the end of the trial.
Dietary Assessment
The participants compiled seven-day food records from Thursday through the following Wednesday. Trained interviewers telephoned the participants to collect parts of the record three times during each seven-day recording period, probing for more detail about meals, portion sizes, and methods of preparation while this information was still fresh in the participants' minds. Interviewers recorded the entire record over the telephone, compared it with the written record provided by the participant, and followed up if necessary. The intake of nutrients was determined from computerized food-composition tables.11
Laboratory Procedures
Plasma levels of total cholesterol and triglyceride (with subtraction of a free glycerol blank) were measured by enzymatic procedures (ABA 200 instrument, Abbott Laboratories).12 , 13 HDL cholesterol was measured by dextran sulfate—magnesium precipitation14 followed by enzymatic determination of cholesterol.12 The level of very-low-density lipoprotein (VLDL) cholesterol was calculated as the level of triglyceride divided by 2.18 (or by 5, with conventional units), unless the level of triglyceride was higher than 3.39 mmol per liter (300 mg per deciliter), in which case VLDL cholesterol was measured by enzymatic methods12 after ultracentrifugation for 18 hours.15 The level of cholesterol was calculated16 as the level of total cholesterol minus the levels of HDL cholesterol and VLDL cholesterol. These measurements were consistently within specified limits as monitored by the Lipid Standardization Program of the Centers for Disease Control and the National Heart, Lung and Blood Institute. HDL2 and HDL3 cholesterol levels were measured by enzymatic methods12 after precipitation by dextran sulfate—magnesium.17 Apolipoproteins A-I and B were measured by rate immunonephelometry (Array, Beckman).18
Coronary Heart Disease Risk Score
We calculated a summary estimate of the risk of coronary heart disease, incorporating changes in total and HDL cholesterol levels and systolic blood pressure, for all participants at base line and after one year, using recently updated risk equations based on data from the Framingham Heart Study and the Framingham Offspring Cohort.19
Statistical Analysis
Analysis of variance was used to compare mean differences between groups. All comparisons are two-tailed.
Results
Telephone interviews and clinic screening of 684 men and 982 women in the San Francisco Bay area who responded to media announcements yielded 132 men with a mean (±SD) body-mass index of 30.7±2.2 and a percentage of body fat of 28.2±4.4 percent and 132 women with a body-mass index of 27.9±2.2 and a percentage of body fat of 35.7±4.7 percent.
After all base-line measurements had been completed, the subjects were randomly assigned to one of the three intervention groups: diet only (45 men and 42 women), diet plus exercise (43 men and 47 women), and control (44 men and 43 women). Ten men did not return for testing after one year, two had incomplete food records, and one had incomplete lipid data. Seventeen women did not return for one-year testing, two of whom had become pregnant, and three other women had incomplete data from food records, hydrostatic weighing, or blood tests. No significant differences with respect to dropouts were found among the three male or three female study groups. The analyses presented here are restricted to the subjects in the diet-only group (40 men and 31 women), the diet-plus-exercise group (39 men and 42 women), and the control group (40 men and 39 women) for whom there were complete data on plasma triglyceride, cholesterol, and lipoprotein levels, seven-day food records, and body composition at base line and after one year. Base-line values for major variables in all the men and all the women included in the analyses are given in Tables 1Table 1
Clinical Characteristics of the Men in the Study at Base Line and after One Year.* and 2Table 2
Clinical Characteristics of the Women in the Study at Base Line and after One Year.*, respectively.Within each sex, the three study groups were well matched at base line for age (men, 40.3±6.3 years; women, 39.1±6.4 years), body composition, aerobic capacity, and the intake of most nutrients. There were no significant differences in systolic blood pressure or levels of triglyceride, HDL cholesterol, HDL2 cholesterol, and apolipoprotein A-I for either sex among the three groups. Slight differences between groups were significant with respect to diastolic blood pressure in men and total and LDL cholesterol levels in both sexes.
Plasma lipoprotein levels associated with an increased risk of coronary heart disease4 were common at base line among these overweight subjects: 77 men (65 percent) and 49 women (44 percent) had a level of LDL cholesterol ≥3.36 mmol per liter (130 mg per deciliter), 30 men (25 percent) and 1 woman (1 percent) had levels of HDL cholesterol <0.91 mmol per liter (35 mg per deciliter).
Effects of the Interventions in Men
As Table 1 shows, both intervention groups lost a significant amount of total body weight and fat weight, as compared with the controls. Adding exercise to the diet increased the loss of fat by 81 percent (P<0.001). Correspondingly, the percentage of body fat was decreased significantly more by diet plus exercise (—7.0 percent) than by diet alone (—3.8 percent, P<0.001). In both intervention groups, as compared with the controls, the ratio of abdomen to hip girth was significantly reduced; the reduction in the diet-plus-exercise group was significantly larger than that in the diet-only group.
The diet-plus-exercise group walked or ran 14.7±8.0 km per week during the 10-month intervention period. Maximal aerobic capacity increased significantly in the diet-plus-exercise group, as compared with both the diet-only and the control groups.
Table 1 shows that both male intervention groups reported a significant reduction in total energy intake, the percentage intakes of total and saturated fats, and the intake of cholesterol, as compared with the control group.
In both intervention groups, but not the control group, systolic and diastolic blood pressure was reduced. The group that combined diet and exercise had significantly reduced triglyceride levels and increased HDL cholesterol, HDL2 cholesterol, and apolipoprotein A-I levels as compared with the control group and the diet-only group, whereas the diet-only group had no significant change in these variables as compared with the control group. Apolipoprotein B levels decreased significantly in both intervention groups as compared with the control group.
There was a significant decrease in the ratio of total plasma cholesterol to HDL cholesterol in both the diet-only group (—0.63–1.15, P<0.01) and the diet-plus-exercise group (—1.04±1.12, P<0.001) as compared with the controls (+0.01±0.78). Figure 1Figure 1
Changes in Lipoprotein and Apolipoprotein Ratios in the Study Groups after One Year. shows the mean changes in the ratios of LDL cholesterol to HDL cholesterol and apolipoprotein B to apolipoprotein A-I. These ratios were significantly decreased in the diet-only and diet-plus-exercise groups as compared with the controls. The decrease in the apolipoprotein ratio was larger in the men assigned to diet plus exercise than in those assigned to diet only.The estimated risk of coronary heart disease was significantly reduced in both intervention groups as compared with the control group, and this reduction was significantly greater in men in the diet-plus-exercise group (—35 percent) than in those in the diet-only group (—23 percent).
Effects of the Interventions in Women
Table 2 shows that in women as well as men both interventions produced significant weight loss (primarily fat). Adding exercise to the diet increased the loss of fat by 38 percent, but the change in the percentage of body fat in women in the diet-plus-exercise group (—5.2 percent) was not significantly different from that in women in the diet-only group (—3.5 percent). As compared with women in the control group, those in the diet-plus-exercise group reduced their ratio of abdominal to hip girth significantly, whereas there was no change in the women in the diet-only group. As compared with both the control and the diet-only groups, the diet-plus-exercise group had significantly increased maximal oxygen consumption. The average distance walked or run per week was only slightly shorter among women (12.5±7.6 km) than among men. Both the diet-only and the diet-plus-exercise groups reported significant reductions in their intakes of total energy and cholesterol and in the percentage of energy from total and saturated fats.
As compared with the controls, the women in both intervention groups had significantly reduced systolic and diastolic blood pressures and total and LDL cholesterol and apolipoprotein B levels. HDL cholesterol and HDL2 cholesterol levels were significantly increased in the diet-plus-exercise group as compared with the diet-only group. Women in the diet-only group had significantly reduced HDL2 cholesterol and apolipoprotein A-I levels as compared with the controls. The women assigned to diet plus exercise had a slight but significant decrease in the level of triglyceride as compared with the controls, but no change in HDL cholesterol (Table 2); however, the ratio of total to HDL cholesterol dropped significantly in the women assigned to diet plus exercise (—0.24±0.47) as compared with both the controls (+0.10±0.50, P<0.01) and the women assigned to diet only (+0.04±0.62, P<0.05). Figure 1 shows that the ratios of LDL to HDL cholesterol and apolipoprotein B to apolipoprotein A-I decreased significantly in the diet-plus-exercise group as compared with the control group but were unchanged in the diet-only group.
The estimated risk of coronary heart disease was significantly reduced in the diet-plus-exercise group as compared with both the control group (—35 percent) and the diet-only group; the reduction in the diet-only group (—20 percent) was not significant as compared with that in the control group.
Changes in Plasma Triglyceride and Lipoprotein Cholesterol Concentrations in Men and Women
The mean changes after one year in the plasma concentrations of triglyceride, LDL cholesterol, and HDL cholesterol are shown as a percentage of the mean base-line levels in all the groups in Figure 2Figure 2
Percent Changes in Plasma Triglyceride and Lipoprotein Cholesterol Concentrations in the Study Groups after One Year..Discussion
This report extends our previous investigation of weight loss induced by exercise as compared with caloric restriction in men1 to a consideration of the optimal prescription for hygienic weight loss to reduce the risk of coronary heart disease in moderately overweight men and premenopausal women. Sedentary living is widespread20 and characteristic of overweight people, whereas increased physical activity and physical fitness promote the loss of fat21 and are strongly associated with a decreased risk of coronary heart disease.22 , 23 The present controlled study promoted a "heart-healthy" (NCEP Step 1) diet to bring about a reduction in energy intake in two intervention groups for each sex: one involved dietary changes alone (the diet-only group) and one involved these dietary changes plus a supervised program of exercise (the diet-plus-exercise group).
Although diet alone significantly reduced body fat after one year in the men, the addition of exercise produced a substantially greater loss. There was also a greater reduction in the ratio of abdominal to hip girth in the men when the exercise component was added. This ratio was also reduced in the exercising women, but not in the women assigned to diet only. The ratio of abdominal to hip girth correlates more strongly with rates of total mortality and mortality from coronary heart disease than traditional measures of adiposity in both men24 and women.25
In our previous study of energy restriction, a significant increase of about 11 percent in HDL cholesterol levels was noted in overweight men who had lost weight over a period of one year on a typical American diet.1 In the present study of energy restriction, HDL cholesterol levels increased by only 2 percent in overweight men who had lost weight over a one-year period on an energy-restricted diet that approximated or exceeded NCEP Step 1 dietary goals. In women who adopted this diet, HDL cholesterol levels decreased by about 7 percent despite loss of weight. The reduced-calorie NCEP Step 1 diet appears to have eliminated the expected beneficial effect of weight loss on the HDL cholesterol level, although a desirable lowering of the LDL cholesterol level (not significant in men) and the apolipoprotein B level was observed in both sexes. In the men, diet plus exercise produced a greater increase in HDL cholesterol than did diet only. In the women, exercise offset the effect of the diet, so that HDL cholesterol levels were not significantly changed as compared with those in the controls.
Some 30 percent of American adults would benefit from weight loss, and the majority of them are appropriate candidates for a prudent diet. Our findings have relevance to the adult treatment guidelines of the NCEP26 (which make no mention of the therapeutic potential of increased exercise), since the increase in the risk of coronary heart disease associated with a reduced level of HDL cholesterol is substantial. Furthermore, in women the HDL cholesterol level has been shown to be a stronger risk factor for coronary heart disease than the LDL cholesterol level.27
In both sexes, the indexes of atherogenic risk — the ratios of LDL to HDL cholesterol and apolipoprotein B to apolipoprotein A-I — both of which have been shown to be strongly associated with coronary heart disease,28 were substantially and favorably influenced by weight loss promoted by diet plus exercise as compared with diet alone or no intervention.
Resting systolic and diastolic blood pressure was reduced significantly and similarly in the men and women in both intervention groups as compared with the control group. These findings are generally consistent with our earlier results9 and those of others,29 and they suggest that weight loss on a fat-reduced prudent diet results in a sustained reduction in blood pressure, even in overweight people who were initially within the normotensive range.
The addition of regular exercise to the hypocaloric diet produced a substantial further reduction in the estimated risk of coronary heart disease19 in both sexes.
The program of moderate exercise used in our study was acceptable to and generally enjoyed by the majority of our overweight participants, and it appears to be realistic for a large proportion of sedentary and overweight people 25 to 49 years old. The substantial improvement in physical fitness achieved by the exercisers suggests important health benefits with respect to several chronic diseases for both old and young adults.23
Supported by a grant (HL-24462) from the National Institutes of Health and a Research Career Development Award (HL-02183) to Dr. Williams.
We are indebted to Darlene Dreon, M.S., R.D., M.P.H., Sharon Bortz, M.S., R.D., and Susan Kayman, Dr.P.H., R.D. for coordination of the nutrition intervention; to Barbara Frey-Hewitt, M.S., for developing and overseeing the exercise program; to Abby King, Ph.D., and Laura Arnold, M.A., for maintaining adherence; to Scott Hake and Walter Bortz for clinical and physiologic testing; to H. Robert Superko, M.D., and Ami Laws, M.D., for medical supervision, to Nancy Ellsworth, Ashley Owen, R.D., and Charlene Kirchner, R.D., for nutritional assessment; to Dana Anderson and Maria Marsh for coordination of subjects; to Karen Vranizan, M.A., Hilda Maibach, M.A., and Richard Terry, Ph.D., for data management and statistical assistance; to Marlene Hunter, M.T., Anne Schiagenhaft, B.S., and the laboratory staff for lipoprotein analyses; to Roselyn Friccero for secretarial and administrative support; to our participants for their cooperation and patience; and to Stephen P. Fortmann, MD., for critical review of the paper.
Source Information
From the Stanford Center for Research in Disease Prevention, Stanford University School of Medicine, Stanford, Calif. Address reprint requests to Dr. Wood at Stanford Center for Research in Disease Prevention, 730 Welch Rd., Palo Alto, CA 94304–1583.
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