Effects of the Amount and Intensity of Exercise on Plasma Lipoproteins
William E. Kraus, M.D., Joseph A. Houmard, Ph.D., Brian D. Duscha, M.S., Kenneth J. Knetzger, M.S., Michelle B. Wharton, M.A., Jennifer S. McCartney, M.A., Connie W. Bales, Ph.D., R.D., Sarah Henes, R.D., Gregory P. Samsa, Ph.D., James D. Otvos, Ph.D., Krishnaji R. Kulkarni, Ph.D., and Cris A. Slentz, Ph.D.
Background Increased physical activity is related to reducedrisk of cardiovascular disease, possibly because it leads toimprovement in the lipoprotein profile. However, the amountof exercise training required for optimal benefit is unknown.In a prospective, randomized study, we investigated the effectsof the amount and intensity of exercise on lipoproteins.
Methods A total of 111 sedentary, overweight men and women withmild-to-moderate dyslipidemia were randomly assigned to participatefor six months in a control group or for approximately eightmonths in one of three exercise groups: high-amount–high-intensityexercise, the caloric equivalent of jogging 20 mi (32.0 km)per week at 65 to 80 percent of peak oxygen consumption; low-amount–high-intensityexercise, the equivalent of jogging 12 mi (19.2 km) per weekat 65 to 80 percent of peak oxygen consumption; or low-amount–moderate-intensityexercise, the equivalent of walking 12 mi per week at 40 to55 percent of peak oxygen consumption. Subjects were encouragedto maintain their base-line body weight. The 84 subjects whocomplied with these guidelines served as the basis for the mainanalysis. Detailed lipoprotein profiling was performed by nuclearmagnetic resonance spectroscopy with verification by measurementof cholesterol in lipoprotein subfractions.
Results There was a beneficial effect of exercise on a varietyof lipid and lipoprotein variables, seen most clearly with thehigh amount of high-intensity exercise. The high amount of exerciseresulted in greater improvements than did the lower amountsof exercise (in 10 of 11 lipoprotein variables) and was alwayssuperior to the control condition (11 of 11 variables). Bothlower-amount exercise groups always had better responses thanthe control group (22 of 22 comparisons).
Conclusions The highest amount of weekly exercise, with minimalweight change, had widespread beneficial effects on the lipoproteinprofile. The improvements were related to the amount of activityand not to the intensity of exercise or improvement in fitness.
Increased physical activity and fitness are clearly associatedwith reductions in the risk of cardiovascular disease,1,2,3,4,5but the optimal intensity or amount of exercise necessary forreductions in risk or risk factors is unknown. Because of apparentlyconflicting information,1,2,3 there is confusion about whatrecommendations to make for exercise that will confer specifichealth benefits. In spite of the importance of this issue, therehave been no prospective studies investigating the effects ofdifferent amounts and intensities of exercise.
Although regular exercise is known to decrease the risk of cardiovasculardisease, comprehensive reviews6,7 suggest that exercise haslittle effect on total cholesterol or low-density lipoprotein(LDL) cholesterol concentrations and only a minimal and inconsistentbeneficial effect on high-density lipoprotein (HDL) cholesterolconcentrations.6 Thus, there are two deficiencies in the currentknowledge in this area. First, the ability to draw conclusionsabout the relation between exercise and lipids is compromisedby the lack of prospective, randomized exercise studies comparingat least two different amounts of exercise.6 Second, it is nowclear that the concentrations of LDL particles, small LDL particles,large HDL particles, and large very-low-density lipoprotein(VLDL) particles are better indicators of cardiovascular riskthan are the elements of the traditional lipid profile.8,9,10,11,12,13,14,15,16,17
The purpose of the Studies of Targeted Risk Reduction Interventionsthrough Defined Exercise (STRRIDE), a randomized, controlledclinical study, was to investigate the effects of the amountand intensity of exercise on risk factors for cardiovasculardisease in overweight and obese men and women with mild-to-moderatedyslipidemia. Here we report the effects on serum lipoproteins.
Methods
Study Design
A complete description of the design of the study has been publishedelsewhere.18 The research protocol was reviewed and approvedby the relevant institutional review boards.
Study Subjects
After giving written, informed consent, 159 subjects, 40 to65 years of age, who were sedentary, were overweight or mildlyobese (body-mass index [the weight in kilograms divided by thesquare of the height in meters], 25 to 35), and had dyslipidemia(either an LDL cholesterol concentration of 130 to 190 mg perdeciliter [3.4 to 4.9 mmol per liter] or an HDL cholesterolconcentration below 40 mg per deciliter [1.0 mmol per liter]for men or below 45 mg per deciliter [1.2 mmol per liter] forwomen), were randomly assigned to one of three exercise groupsor a nonexercising control group. Subjects were recruited continuouslybetween January 1999 and June 2000, and the exercise programwas completed by April 2001. Of the 159 randomized subjects,48 (30.2 percent) dropped out of the study, 15 (9.4 percent)had an excessively low rate of adherence to exercise, 10 (6.3percent) had incomplete lipid data, and 2 (1.3 percent) hadexcessive weight loss, leaving 84 subjects in the main analysis.
Exercise Training
The exercise prescriptions in the three exercise groups wereas follows: high-amount–high-intensity exercise, the caloricequivalent of jogging approximately 20 mi (32.0 km) per weekfor a person weighing 90 kg (range, 19.2 to 20.6 mi [30.7 to33.0 km] per week for a person weighing 70 to 110 kg)19 at 65to 80 percent of peak oxygen consumption; low-amount–high-intensityexercise, the caloric equivalent of jogging approximately 12mi (19.2 km) per week at 65 to 80 percent of peak oxygen consumption;and low-amount–moderate-intensity exercise, the caloricequivalent of walking approximately 12 mi per week at 40 to55 percent of peak oxygen consumption. For the subjects in thehigh-amount–high-intensity group, the specific prescriptionwas to expend 23 kcal per kilogram of body weight per week;subjects in the two low-amount groups were to expend 14 kcalper kilogram per week. The machines used for exercise includedcycle ergometers, treadmills, and elliptical trainers. Therewas an initial period of two to three months during which theamount and intensity of exercise were gradually increased, followedby six months at the appropriate exercise prescription. Allexercise sessions were verified by direct supervision or byheart-rate monitors that provided recorded data (Polar Electro).
Dietary Evaluations and Control of Body Weight
Nutrient intakes were determined at base line and at the endof the study. To minimize the confounding effects of weightloss, subjects were counseled to maintain body weight, whichwe believed to be ethically justified by the short time frameof the study. Data were excluded from the primary analysis forsubjects whose weight varied by more than 5 percent from baseline to the end of the study.
Lipids and Lipoproteins
Fasting plasma samples were analyzed by LipoScience for lipoproteinprofiling by nuclear magnetic resonance spectroscopy. Each measurementincludes the concentrations of six subclasses of VLDL, foursubclasses of LDL (including intermediate-density lipoprotein[IDL]), and five subclasses of HDL, as well as the calculatedweighted average sizes of VLDL, LDL, and HDL particles, theconcentration of LDL particles, and estimates of total cholesterol,triglycerides, LDL cholesterol, and HDL cholesterol concentrations.20,21Since the nuclear magnetic resonance imaging method measureslipoprotein particles rather than cholesterol, we sought verificationof findings using a method that directly measures cholesterolin lipoprotein fractions separated by density-gradient ultracentrifugation.22Samples from 20 subjects (10 men and 10 women) in the high-amount–high-intensitygroup and 20 subjects in the control group were analyzed byAtherotech (Birmingham, Ala.) with the Vertical Auto Profilemethod.22 All samples sent for lipid and lipoprotein analysisdid not indicate the treatment-group assignment of the subject.
Intention-to-Treat Analysis
The goal of our study was to determine the physiological effectsof specific, well-defined amounts and intensities of exerciseon risk factors for cardiovascular disease. The study was specificallydesigned to address the questions of "How much exercise is enough?"and "What is the optimal amount of exercise?" with respect topotentially beneficial effects on cardiovascular health anddisease. To these ends, and in order to maintain clear separationsof the levels of exercise among the exercise groups, we definedacceptable compliance rates for subjects in all exercise groupsa priori to be between 74 percent and 115 percent of the assignedamount of exercise, thus permitting study of the relation betweenthe actual level of exercise (not necessarily the intentionto exercise) on various health-related variables. For similarreasons related to the effects of weight on lipoproteins, wealso excluded subjects from the main analysis if they had achange in weight of more than 5 percent over the course of thestudy. Nevertheless, there may be clinical implications of anintention-to-treat analysis, and we therefore also report theresults of such an analysis including all 101 subjects who hadcomplete lipid data, irrespective of compliance or weight change.
Statistical Analysis
For the main analysis, we used analysis of variance (Statviewor SAS software) followed by post hoc analysis. Unless indicated,only the results of post hoc analyses are reported. Becauseof the primary a priori interest, only differences between eachexercise group and the control group were analyzed. An alphaerror of less than 0.0167 was considered to indicate statisticalsignificance, because of Bonferroni's correction.
To test for hypothesized effects of the amount and intensityof exercise, we used a multivariate analysis of variance totest for differences between the groups with regard to the entireset of 11 variables. We then ranked (for each variable) thegroups with different amounts of exercise and, separately, thegroups with different intensities of exercise. The group withthe largest improvement was ranked first, and so on.
Results
Base-line characteristics of the subjects are presented in Table 1.There were no significant differences among the groups interms of demographic variables or in terms of initial fitness,total caloric intake, or macronutrient intake. Subjects whodropped out of the study were not significantly different fromthose who remained in the exercise or control groups in termsof age, height, weight, or body-mass index (data not shown).
Table 1. Base-Line Characteristics of the Subjects, Characteristics of Their Exercise Programs, and Changes in Body Weight, Fitness, and Nutrient Intake.
Level of Exercise and Fitness Responses
A description of the exercise prescriptions and the effectsof exercise on body weight, cardiovascular fitness (peak oxygenconsumption), and nutrient intake are also shown in Table 1.In spite of the monitoring of body weight and the recommendationto maintain body weight, subjects in the high-amount–high-intensityand low-amount–moderate intensity groups had weight lossthat was small but significantly greater than that among controls.The high-amount–high-intensity and low-amount–high-intensitygroups had similar increases in peak oxygen consumption (17.8percent and 16.7 percent, respectively; P<0.001 for bothcomparisons with the control group), implying that the intensityof exercise is more important than the amount of exercise interms of increasing the level of fitness. There were no significantdifferences among groups in terms of changes in caloric consumptionor the percentage of calories from macronutrients.
Base-Line Differences and Outliers
Lipoprotein data obtained at base line and at the end of thestudy are shown in Table 2. The low-amount–moderate-intensitygroup had significantly higher base-line concentrations of triglyceridesand large VLDL particles than did controls. When the data wereinspected for outliers, three subjects in the low-amount–moderate-intensitygroup were identified. When subsequent analyses were performedboth with and without these subjects, the overall interpretationof the data was unchanged. Therefore, data from all qualifyingsubjects were included in all analyses.
Figure 1. Comparison of the Effects of Three Different Exercise Programs with Those in a Control Group on Mean Changes in the Concentration of Small Low-Density Lipoprotein (LDL) Cholesterol (Panel A), the Concentration of LDL Particles (Panel B), the Average Size of LDL Particles (Panel C), and the Concentration of Intermediate-Density Lipoprotein (IDL) Cholesterol (Panel D).
Subjects in the control group maintained their normal diet and level of physical activity for six months. In the exercise groups, the amount and intensity of exercise were gradually increased to the prescribed level over the course of one to three months, after which exercise was maintained at the prescribed level for six months. Low-amount–moderate-intensity exercise represents the caloric equivalent of walking approximately 12 mi per week at 40 to 55 percent of peak oxygen consumption; low-amount–high-intensity exercise represents the same amount of exercise at 65 to 80 percent of peak oxygen consumption. High-amount–high-intensity exercise represents the caloric equivalent of jogging approximately 20 mi per week at 65 to 80 percent of oxygen consumption. Values shown represent means of individual change scores. I bars represent the standard errors. To convert the values for cholesterol to millimoles per liter, multiply by 0.02586.
This effect of the amount of exercise was also seen for HDLvariables, as shown in Figure 2. There was a clear beneficialeffect (P<0.0167) on the HDL cholesterol concentration inthe high-amount–high-intensity group. The lower amountof exercise had smaller (nonsignificant) effects on these variables,with no apparent effect of the intensity of exercise.
Figure 2. Comparison of the Effects of Three Different Exercise Programs with Those in a Control Group on Mean Changes in Total High-Density Lipoprotein (HDL) Cholesterol Concentration (Panel A), Concentration of Large HDL Cholesterol (Panel B), and Average Size of HDL Particles (Panel C).
I bars represent the standard errors. To convert the values for cholesterol to millimoles per liter, multiply by 0.02586.
In the high-amount–high-intensity, low-amount–high-intensity,and low-amount–moderate-intensity groups, there was improvementin triglyceride concentration (P=0.006, P=0.07, and P<0.001,respectively), concentration of VLDL triglycerides (P=0.004,P=0.04, and P<0.001, respectively), concentration of largeVLDL particles (P=0.05, P=0.13, and P<0.001, respectively),and size of VLDL particles (P=0.06, P=0.005, and P<0.001,respectively).
Ranked Effects of the Intensity and Amount of Exercise
The ranked effects of the amount and intensity of exercise areshown in Table 3. The test for overall differences among groupswas statistically significant according to multivariate analysisof variance (P=0.03), providing a rationale for examining theeffect of the amount of exercise. High-amount–high-intensityexercise had a larger effect on 10 of the 11 variables thandid low-amount–high-intensity exercise. In turn, low-amount–high-intensityexercise had a beneficial effect on all 11 variables, as judgedby comparisons with the control group. These findings demonstratea clear effect of the amount of exercise: in 21 of 22 cases,the higher the level of exercise, the greater the effect onlipid measures. The rankings of the levels of intensity showthat neither low-amount–high-intensity exercise nor low-amount–moderate-intensityexercise was clearly superior in its effects on lipoproteins.The data therefore suggest that there is no clear effect ofthe intensity of exercise. However, both low-amount groups rankedabove the control group on all 11 variables.
Table 3. Effects of the Amount and Intensity of Exercise on Lipids, Lipoproteins, and Lipoprotein Subfractions.
Intention-to-Treat Analysis
The conclusions from the intention-to-treat analyses (Table 4)were nearly identical to those from the primary analysis.In some cases, the intention-to-treat analysis revealed significantdifferences (P<0.0167) between groups in comparisons forwhich only nonsignificant differences were found in the primaryanalysis. Conversely, in no case did the intention-to-treatanalysis yield nonsignificant differences for comparisons thatyielded statistically significant differences in the primaryanalysis. In sum, an intention-to-treat analysis would haveprovided stronger evidence than the primary analysis did ofthe benefits of high-amount–high-intensity exercise overthe control condition. For example, according to the intention-to-treatanalysis, P=0.002 for the comparison between the high-amount–high-intensitygroup and the control group in terms of the concentration ofsmall LDL particles, P=0.001 for the comparison of the sizeof LDL particles, P=0.02 for the comparison of the concentrationof LDL particles, P=0.06 for the comparison of the IDL cholesterolconcentration, P=0.01 for the comparison of the HDL cholesterolconcentration, P=0.04 for the comparison of the concentrationof large HDL particles, and P=0.02 for the comparison of thesize of HDL particles.
Table 4. Intention-to-Treat Analysis of Effects of the Amount and Intensity of Exercise on Plasma Lipoproteins as Measured by Nuclear Magnetic Spectroscopy.
Reproducibility of Findings with the Use of Density-Gradient Ultracentrifugation
Because of the relative novelty of the various measurement techniquesfor the analysis of lipoprotein subfractions, we thought itimportant to confirm our findings using a complementary technique.We tested the same hypotheses in 40 subjects (20 in the high-amount–high-intensitygroup and 20 in the control group) using density-gradient ultracentrifugationcombined with direct spectrophotometric measurement of cholesterolin all lipoprotein subfractions.22 The results of the analysesand the conclusions regarding the changes in lipoprotein measurementswere similar with the two techniques (data not shown).
Discussion
Our study compared the effects of two different amounts andintensities of exercise training on lipoproteins in a prospective,randomized, controlled manner. The data show a clear effectof the amount of exercise on lipoproteins and lipoprotein subfractions;they also show that a relatively high amount of regular exercise— even in the absence of clinically significant weightloss — can significantly improve the overall lipoproteinprofile. In particular, the data reveal that exercise at a caloricequivalent of 17 to 18 mi (27.2 to 28.8 km) per week and anintensity equivalent to that of jogging at a moderate pace significantlydecreased the concentrations of small LDL and LDL particlesand increased the average size of LDL particles, without changingthe plasma LDL cholesterol concentration. This amount of exercisealso increased the total HDL concentration, the concentrationof large HDL particles, and the average size of HDL particlesand decreased the concentrations of triglycerides and totalVLDL triglycerides with decreases in the IDL concentration,the concentration of large VLDL particles, and the average sizeof VLDL particles that were at the margin of statistical significance(P<0.07). These findings were confirmed and strengthenedin a parallel intention-to-treat analysis. None of these improvements,except for those in HDL cholesterol and triglycerides, wouldhave been detected by the standard lipid panel. These data refutethe general conclusion, based on results from the standard lipidpanel and on studies in which moderate amounts of exercise (similarto that in the low-amount groups in our study) were used, thatexercise has only limited effects on lipids and lipoproteins.6
The second major finding is that the amount of exercise appearsto make a greater difference than the intensity of exerciseon plasma lipoprotein concentrations. Our data agree with thoseof Duncan et al.,23 in which three walking groups (strollers,brisk walkers, and aerobic walkers) exercised the same amount(approximately 13 mi [20.8 km] per week) for 24 weeks. The strollersand aerobic walkers had improvements of 6 percent and briskwalkers an improvement of 4 percent in the HDL cholesterol concentration.Several studies have shown that low-intensity exercise can resultin improvements in lipoproteins.23,24,25,26 Our data, takentogether with those of others, suggest that any effect on lipidsof the intensity of exercise is small as compared with thatof the amount of exercise. A high-amount–moderate-intensitygroup was not included in our study because of the very largeweekly time commitment that would have been required (up toeight hours for subjects with a low level of fitness). Thus,we cannot exclude the possibility that the level of intensitywould have an effect in subjects with higher amounts of exercise.
Cross-sectional studies have reported that runners have smalleramounts of atherogenic small LDL particles than do controlswho do not exercise.27,28 However, in those studies, the percentageof body fat was significantly higher among the sedentary subjects,potentially confounding the results. In an exercise study, Williamset al.29 reported no difference between subjects randomly assignedto exercise and controls in any changes in LDL or VLDL subfractions.These findings were most likely due to the small average amountof exercise of only about 8 mi (12.8 km) per week. When theinvestigators examined the correlation between the concentrationof small LDL particles and the distance run by subjects withinthe running group, they found a significant, albeit small, inverserelation. It is important to note that weight loss was permittedin that study, and the investigators ascribed most of the changeto weight loss. Several studies have reported significant effectsof exercise on lipoproteins. However, in those studies, exerciseinduced larger weight losses than those seen in our study, andthe effect was generally attributed to or correlated with weightloss.29,30,31,32,33 In our study, we were able to minimize greatly,although not to eliminate completely, weight differences andweight loss as confounding factors.
Some additional conclusions are warranted. First, although thelower amount of exercise resulted in fewer significant improvements,this amount of exercise was able to limit or prevent in thelow-amount groups much of the weight gain and consequent worseningof the overall lipoprotein profile that was observed in thecontrol group. Second, although the two high-intensity groupshad very similar increases in fitness (as measured by peak oxygenconsumption), only the high-amount group had extensive improvementsin the overall lipoprotein profile. Similarly, the same lowamount of weekly exercise had very different effects on fitnessin the high-intensity group and the moderate-intensity groupbut had similar effects on the lipoprotein profile in the twogroups. Therefore, it would appear that it is the amount ofactivity — and not necessarily the change in fitness —that is important for the improvement of the lipoprotein profilewith exercise programs.
In conclusion, our study demonstrates that regular exercisewith minimal weight change has broad beneficial effects on thelipoprotein profile. A clear, biologically consistent associationemerged between the amount of exercise and the degree of improvementin the lipoprotein profile, with the higher amount of exercise(equivalent to 17 to 18 mi of jogging at a moderate pace perweek) having a much greater beneficial effect on lipids andlipoproteins than the lower amount of exercise (equivalent tojogging or walking approximately 11 mi per week). The loweramount of exercise prevented the weight gain seen in the controlsand was clearly more beneficial for the lipoprotein profilethan was a sedentary lifestyle. The greater amount of exercisewas approximately that which, according to the initial results,provided the maximal benefit in preventing cardiovascular eventsand death from any cause among subjects in the Harvard AlumniStudy.34 The extensive improvements achieved in the high-amount–high-intensitygroup were related to the amount of physical activity and didnot appear to be related to changes in the level of fitness.Finally, the intensity of exercise was less important, at leastin the case of the lower amount of exercise studied, than theamount of exercise in terms of lipoprotein responses.
Supported by a grant (HL-57354) from the National Institutesof Health.
Dr. Otvos reports being an employee, officer, and stockholderof LipoScience.
Dr. Kulkarni reports being an employee of Atherotech and havingoptions for the purchase of stock. He also receives royaltiesas an inventor of the Vertical Auto Profile technology.
Source Information
From the Divisions of Cardiology (W.E.K., B.D.D., K.J.K., C.A.S.), Geriatrics (C.W.B., S.H.), and General Internal Medicine (G.P.S.), Department of Medicine, the Duke Center for Living (W.E.K.), the Center for Health Policy Research (G.P.S.), and the Department of Community and Family Medicine (G.P.S.), Duke University Medical Center; and the Geriatric Research, Education, and Clinical Center, Durham Veterans Affairs Medical Center (C.W.B.) — both in Durham, N.C.; the Department of Exercise and Sport Science and the Human Performance Laboratory, East Carolina University, Greenville, N.C. (J.A.H., M.B.W., J.S.M.); LipoScience, Cary, N.C. (J.D.O.); and Atherotech, Birmingham, Ala. (K.R.K.).
Address reprint requests to Dr. Kraus at the Division of Cardiology, Department of Medicine, P.O. Box 3327, Duke University Medical Center, Durham, NC 27710, or at william.kraus{at}duke.edu.
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50 years) and women (
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