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Medicine & Science in Sports & Exercise:
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Response of blood lipids to exercise training alone or combined with dietary intervention

LEON, ARTHUR S.; SANCHEZ, OTTO A.

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Laboratory of Physiological Hygiene and Exercise Science, Division of Kinesiology, College of Education and Human Development; and Heart Disease Prevention Clinic, Division of Cardiology, The Medical School, University of Minnesota, Minneapolis, Minnesota 55455

Submitted for publication January 2001.

Accepted for publication March 2001.

Proceedings for this symposium held October 11–15, 2000, Ontario, Canada.

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Abstract

LEON, A. S., and O. A. SANCHEZ. Response of blood lipids and lipoproteins to exercise training alone or combined with dietary intervention. Med. Sci. Sports Exerc., Vol. 33, No. 6, Suppl., pp. S502–S515, 2001.

Purpose: The purpose of this study is to review the effects of aerobic exercise training (AET) on blood lipids and assess dose-response relationships and diet interactions.

Methods: We reviewed papers published over the past three decades pertaining to intervention trials on the effects of ≥ 12 wk of AET on blood lipids and lipoprotein outcomes in adult men and women. Included were studies with simultaneous dietary and AET interventions, if they had appropriate comparison groups. Studies were classified by the participants’ relative weights expressed as mean BMIs. Information was extracted on baseline characteristics of study subjects, including age, sex, and relative baseline cholesterol levels; details on the training programs; and the responses to training of body weight, V̇O2max, and blood total cholesterol (TC) and low-density lipoprotein-cholesterol (LDL-C), high-density lipoprotein-cholesterol (HDL-C), and triglyceride (TG).

Results: We identified 51 studies, 28 of which were randomized controlled trials. AET was generally performed at a moderate to hard intensity, with weekly energy expenditures ranging from 2,090 to >20,000 kJ. A marked inconsistency was observed in responsiveness of blood lipids. The most commonly observed change was an increase in HDL-C (with reductions in TC, LDL-C, and TG less frequently observed). Insufficient data are available to establish dose-response relationships between exercise intensity and volume with lipid changes. The increase in HDL-C with AET was inversely associated with its baseline level (r = −0.462), but no significant associations were found with age, sex, weekly volume of exercise, or with exercise-induced changes in body weight or V̇O2max.

Conclusion: Moderate- to hard-intensity AET inconsistently results in an improvement in the blood lipid profile, with the data insufficient to establish dose-response relationships.

During the past three decades, there have been tremendous advances in the understanding of the role of blood lipids in the pathogenesis of atherosclerosis, the underlying cause of coronary heart disease (CHD), and related cardiovascular diseases (15). The 27th Bethesda Conference of the American College of Cardiology categorized LDL-cholesterol (LDL-C), HDL-cholesterol (HDL-C), and triglycerides (TG) in risk factor categories I, II, and III, respectively (i.e., as risk factors for which interventions have been “proven to” (Category I), “are likely to” (Category II), or “might” (Category III) reduce incidence of CHD events (52). LDL, the principal carrier of cholesterol in the blood, plays a pivotal role in atherogenesis (62), with CHD risk progressively increasing with levels > 2.6 mmol·L-1 (>180 mg·dL- 1). The National Cholesterol Education Program (NCEP) (47) classifies a total cholesterol (TC) level of ≥ 6.2 mmol·L- 1 (>240 mg·dL- 1) and an LDL-C level of ≥ 4.1 mmol·L- 1 (>160 mg·dL- 1) as elevated, and TC levels of 5.2 mmol·L- 1 to 4.0 mmol·L-1 (200–239 mg·dL- 1) and LDL-C levels of ≥ 34 mmol·L- 1 (130 mg·dL- 1) as borderline high. In the presence of CVD or two or more other risk factors, borderline levels of TC and LDL-C are considered elevated. HDL-C appears to be independently and inversely related to severity of atherosclerosis and risk of CHD with levels ≤ 0.9 mmol·L- 1 (≤35 mg·dL- 1) classified as “low” and levels ≥ 1.6 mmol·L-1 (≥60 mg·dL) as a “negative risk factor” or a protective factor against CHD (15,47,50). The possible independent relationship of plasma TG (and its principal carrier in the fasting state, very low density lipoprotein (VLDL)) to CHD is more complex and controversial (15,18,22,50). This is because elevated or borderline high levels of TG (>4.5 mmol·L-1 or >400 mg·dL- 1 and 2.26–4.52 mmol·L- 1 or 200–400 mg·dL- 1, respectively) generally do not occur as isolated entities. More commonly, they are associated with other metabolic disturbances and risk factors, including reduced HDL-C (15,23,50). TG-rich lipoprotein remnants also appear to be atherogenic, but less so than LDL (29,50).

A consensus also exists that physical inactivity and reduced cardiorespiratory endurance contribute to risk of CHD (49,53,79), with a sedentary lifestyle rated in Category II by the 27th Bethesda Conference (52). Among the multiple proposed mechanisms for the postulated protective effect of regular physical activity against CHD is a favorable effect on blood lipids, particularly an increase in HDL-C and a reduction in TG levels (50,54, 79). Evidence supporting this relationship has come from cross-sectional and longitudinal epidemiologic observational studies, as well as a growing number of experimental exercise training studies, and is further supported by small-scale metabolic studies demonstrating mechanisms for observed lipid changes. Such studies, which involved healthy, normal-weight, and obese men and women of all ages, as well as patients with diabetes, hypertension, and CHD, have previously been reviewed during the past two decades (5,8,13,17,38,39,45,54,67,69,76–78).

Cross-sectional observational studies, involving men and women of all ages performing a variety of aerobic activities, have consistently demonstrated what appears to be a positive dose-response association between volume and intensity of aerobic activities and plasma HDL-C levels and inverse associations with TG levels; however, causative relationships cannot be proven by such studies because of numerous potential confounding variables. These include possible genetic factors contributing to both a favorable lipid profile and self-selection of active lifestyles, and especially the contribution of a lower total body and abdominal fat mass in the more active individuals to increased HDL-C and reduced TG levels (13,38,66,81).

The focus of this review is on the results of published studies, which evaluated the effects of supervised endurance exercise conditioning programs on blood lipid and lipoprotein concentrations with identification of those that are randomized controlled trials (RCT). Specific questions that are addressed in this report include the following: 1) Does the available evidence support the hypothesis that endurance exercise training has a favorable influence on the blood lipid profile relative to future risk of CHD? 2) Does the blood lipid responses to training differ by the study subjects’ sex, age, or race/ethnicity, and baseline lipid levels, and baseline relative body weight and its change with training? 3) Are the lipid responses to exercise related to the intensity, duration, the weekly volume of energy expenditure, the length of the endurance exercise program, and the associated changes with training in maximal oxygen uptake (V̇O2max)?

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METHODS

For this review, an English language literature search from 1987 to the present was conducted via MEDLINE (National Library of Medicine, Bethesda, MD) and the Index Medicus, using as key words physical activity, exercise, blood lipids, and lipoproteins alone or in combination. Additional studies, particularly those published before 1987, were identified from references by previous reviewers. Since a consensus already exists that at least 12 wk of endurance exercise is required to have a training effect on blood lipids (49,66), this review was limited to studies of at least this length. Unless otherwise indicated, in the studies summarized in Tables 1–3, interventions consisted of supervised structured group aerobic exercise programs in sedentary, apparently healthy, white individuals. Included in these tables are a few studies in which monitored “lifestyle activities” and/or home exercises were also prescribed. A few studies also included resistance training.

Table 1
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Table 2
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Table 2
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Table 2
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Table 2
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Table 3
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Table 3
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A total of 51 studies were identified that met the above inclusion criteria. Of these, 28 were RCT. The studies are classified in Tables 1–3 by the participants’ pretraining mean body mass index (BMI) levels, a format previously used by Stefanick (67). The BMI cutoff points of <25.0 kg·m-2 in Table 1, 25.0–29.9 kg·m-2 in Table 2, and ≥ 30 kg·m- 2 in Table 3 are consistent with recent NHLBI Expert Panel recommendations for classifying people as normal weight, overweight, or obese, respectively (49). Studies cited are listed in chronological order and include the following information: number of subjects completing the studies, and their sex, age, and race/ethnicity if other than white; classification of baseline blood cholesterol and LDL-C levels on the basis of on NCEP guidelines (47); and any special health-related characteristics such as whether there was a nonexercise control group; details on the exercise training program, i.e., type(s) of exercise, length of the program, the peak intensity, frequency, and duration of exercise sessions, length of training, and an estimate of the weekly volume of energy expenditure, obtained either directly from published information, or more frequently calculated from the type of activity and the exercise prescription using the Ainsworth et al. (1) compendium of energy cost of specific activities and other interventions. Posttraining outcomes, in addition to whether there were any significant changes in TC, LDL-C, HDL-C, and TG, included changes in body weight and relative improvement in V̇O2max. Improvement in V̇O2max (mL·min- 1) was classified as low (<10%), moderate (11–19%), or high (≥20%). Exercise-induced change in body weight and blood lipids were compared by two-tailed t-tests for statistical significance with either the changes with training in the control group in the RCT or with baseline levels in uncontrolled studies.

We also attempted to identify from the study reports factors related to the study design, which may have affected blood lipid findings. These potential confounding variables included stability of diet and physical activity outside the study; hormonal status of women participants; the timing of the posttraining blood specimens for lipid assays relative to the last training session; and whether adjustments were made for possible plasma volume changes with training. The timing of blood samples relative to the last exercise session is relevant, since research has shown that a single prolonged exercise session may result in plasma volume alterations and acute metabolic responses, which can persist for up to 48 h after exercise (8,13,43,54,69). Reported lipid responses to acute endurance exercise include an increase in plasma HDL-C and a reduction in TG levels.

The strength of linear associations between percent change in the blood lipid/lipoprotein parameters and baseline and posttraining variables was made by Pearson product-moment correlation coefficients with statistical significance established at P < 0.05. Stepwise, multiple linear regression analyses also were performed to determine the percentage of the variability in blood lipid response to training that could be explained by baseline and posttraining variables.

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RESULTS

The 51 studies uncovered in this literature search, of which 28 were randomized RCT, are summarized in Tables 1–3 on the basis of the participants’ baseline mean BMI categories. There were approximately 4700 participants (about 60% men), ranging in age from 18 to 80 yr (mean, 46.6 ± 0.35 yr), who successfully completed these studies. Study participants were predominately white, with only two studies including a sizable number of black subjects (35,44) and only two Asian subjects (46,72). On the basis of NCEP criteria (47), pretraining TC levels were classified as “elevated” in only nine of these studies (8,21,25,37,44,55,60,72,85), and in the remainder they were classified as either “normal” or “borderline high.” Overall mean baseline lipid levels across studies were as follows: TC, 5.29 ± 0.85 mmol·L-1 (204.5 ± 33.9 mg·dL-1); LDL-C, 3.53 ± 0.58 mmol·L-1 (136.5 ± 22.5 mg·dL-1); HDL-C, 1.18 ± 0.24 mmol·L-1 (45.6 ± 9.3 mg·dL-1); and TG, 1.41 ± 0.31 mmol·L-1 (125.0 ± 27.8 mg·dL-1).

In almost all studies, exercise training was performed at a moderate to hard intensity, three to five times per week for 30 min or more per session, consistent with current ACSM guidelines for improving cardiorespiratory endurance in healthy adults (2). Only a limited number of studies directly compared the effects of more than one intensity of exercise on the blood lipid profile (8,11,31,49,70,74,85). The estimated weekly energy expenditure during structured exercise programs ranged from 2,090 kJ·wk-1 to >20,000 kJ·wk-1 (500 to >5,000 kcal·wk-1), with a mean of 5,894.4 ± 3,450.5 kJ·wk-1 (1,408.8 ± 8,24.7 kcal·wk-1) per study. None of the reported studies compared the effects of different volumes of exercise on blood lipids. Theduration of exercise training ranged from 12 wk to 2 yr. Training generally resulted in significant improvements in V̇O2max ranging from <3% to over 50%, with the mean increase across studies of 15.7%.

There was a considerable variability in body weight changes during training depending on whether there were concomitant dietary interventions. In a total of about 2200 subjects from 61 study groups in which there were no concomitant dietary changes, the change in body mass ranged from none to 7.2 kg, with a mean (± SD) change of −0.82 ± 1.38 kg. In contrast, in 15 studies involving overweight or obese subjects in which there were concomitant dietary interventions, the observed weight loss ranged from 7.2 to 17.9 kg.

A marked inconsistency in the response of blood lipids and lipoproteins to endurance exercise training was observed in all three weight categories. The most commonly observed lipid change was a significant (P < 0.05) increase in HDL-C. This was observed in men and women of all ages in 24 of the 51 studies (47%), including 20 studies without simultaneous dietary manipulations. In training groups (N = 61 involving about 2200 subjects) in which diet was held constant, the exercise-induced change in HDL-C ranged from a decrease of 5.8% to an increase of about 25%, with a mean increase of 4.6% across these studies (P < 0.05). Increases in HDL-C with training is reported to primarily involve the HDL2 fraction and to be generally associated with an increase in lipoprotein lipase activity (13,43). Significant reductions in HDL-C levels were observed in two of the training studies reviewed involving overweight or obese participants in which there was a concomitant reduction in fat intake via a NCEP diet (21,37). It has been well documented by feeding experiments that a reduced saturated fat intake in addition to reducing targeted LDL-C also is likely to reduce HDL-C (and raise TG) levels in both black and white subjects (16,24). Observational studies also have shown that populations consuming low-fat diets have both low HDL-C and LDL-C; however, they also invariably have low CHD rates (35). Furthermore, it appears from this review that aerobic exercise training negates or attenuates this dietary-induced reduction in HDL-C, particularly if there is an associated substantial weight loss, i.e., ≥ 4 kg (25,68,85).

Significant reductions in LDL-C, TG, and TC with exercise training were observed less frequently than an increase in HDL-C. Exercise training in the absence of simultaneous dietary interventions resulted in mean reductions in TG, LDL-C, and TC of about 3.7% (P < 0.05), 5.0% (P < 0.05), and 1.0% (P = NS), respectively, across studies. Men generally had a greater reduction in TG levels than the women participants. Concurrent reductions in dietary fat intake and/or a hypocaloric diet potentiated the reduction in these three lipid parameters;however, as previously mentioned, a concomitant reduction in fat intake also reduced HDL-C levels, with the reduction being partially attenuated by simultaneous exercise training and/or weight reduction. Thus, this review confirms the observations of previous reviewers of a marked inconsistency in blood lipid changes with endurance exercise training with an increase in HDL-C noted in only about half of the reported studies. A great deal of heterogeneity in the response to the same training stimulus also has been observed within studies. For example, in the HERITAGE Family Study (43) summarized in Table 2, 20 wk of a standardized and supervised exercise program in a large heterogeneous population resulted in a mean increase is HDL-C of 3.6%; however, further analyses showed that the change ranged from a reduction in HDL-C from baseline levels of 0.11 mmol·L-1 (4.2 mg·dL-1) or 9.3% in Quartile 1 to an increase of 0.18 mmol·L-1 (6.9 mg·dL-1) or 18% in Quartile 4 (Leon et al., unpublished data). This heterogeneity in response was similar for both sexes, blacks and whites, and offspring and parents.

A myriad of potential confounding variables, undoubtedly contributing to this variability in responsiveness of blood lipids to exercise training, are summarized in Table 4. Space limitations prohibit a detailed discussion of how these potential confounding variables may have influenced the outcomes of the studies summarized in this report. However, it should be pointed out that genetic variations are most likely important contributors to this variability. For example, in the HERITAGE Family Study, heritability was found to be a relatively strong contributor to both baseline blood lipids (9) and their responsiveness to exercise training (Rice et al., unpublished data). In addition, methodological flaws were noted in many of the studies surveyed in this report. These include absence of a control group to detect possible laboratory drift andseasonal fluctuations in blood lipid levels; only single blood specimens being obtained before and after training with the timing of the posttraining specimen often ≤ 24 h after the last exercise sessions (and therefore perhaps reflecting lipid changes caused by acute plasma volume or metabolic changes) and over half of the listed studies not even reporting the timing of the posttraining specimen(s); failure to consider the phase of the menstrual cycle in drawing blood before and after training in all but a limited number of the studies involving eumenorrheic women (43,55,59); failure to adjust for possible exercise-induced plasma volume changes in most studies; and possible inadequate control in dietary habits, alcohol intake, smoking, and levels of routine daily physical activity levels during the exercise training phase. The importance of monitoring physical activity aside from the exercise program is illustrated in a study in Table 2 by Leon et al. (40) designed to provide 2000 kcal·wk-1 (8370 kJ·wk-1) of aerobic exercise. Repeated leisure-time physical activity (LTPA) questionnaires revealed that the participants had substantially reduced their usual LTPA during the exercise program, which probably contributed to the failure to achieve a lipid response.

Table 4
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Table 5 shows Pearson correlation values (r) between percent changes in blood lipid parameters and baseline and posttraining variables. This analysis is limited to groups from the studies listed in Tables 1–3, which performed exercise without concomitant dietary changes (N = 61 involving about 2200 subjects). A significant (two-tailed) inverse association was found between the change in HDL-C with training and baseline HDL-C (r = −0.462). The association was even stronger in studies reporting significant increases in HDL-C with training (r = −0.676). This finding is in agreement with that of the HERITAGE Family Study (43); however, a few studies have reported contradictory findings, i.e., that subjects with reduced baseline HDL-C levels were less likely to respond to training (82,86). The only other significant univariate association with increased HDL-C was with a change in LDL-C with training (r = −0.402). No significant associations were observed with weekly energy expenditure during the exercise programs, probably because in almost all of the studies the training volume exceeded the threshold of 3347–4184 kJ·wk-1 (800–1,000 kcal·wk-1) postulated to be required to raise HDL-C (13,38), or with training intensity, session duration, or length of the training program. Also, no significant associations were observed between change in HDL-C and changes with training in body weight, V̇O2max, or with change in TG across studies. However, all lipid parameters generally improved in studies in which there was a substantial weight loss (≥4 kg), usually associated with a concomitant hypocaloric diet. The HERITAGE Family Study (43) also failed to find significant associations between change in HDL-C and change in V̇O2max and body weight with exercise training. Change in TC with training was inversely related to baseline LDL-C levels (r = −0.420), whereas change in TG was associated with baseline levels of body weight (r = 0.435), TG (r = −0.290), and HDL-C (r = 0.348), and with change with training in TC (r = 0.550) (all P < 0.01). Stepwise multiple linear regression analyses also were performed on data from intervention studies limited to exercise alone using the percent changes from before to after training in lipid parameters as dependent variables. Independent variables entered included age and sex; baseline levels of BMI, V̇O2max, and blood lipids; kilojoules per week of exercise performed; and changes after training in body weight, V̇O2max, and blood lipids. The only predictors accepted in the models for changes in HDL-C were baseline HDL-C level and the training-induced change in LDL-C level with the r2 = 0.436 (P < 0.003). The corresponding r2 for the percent change in TC with training was 0.744 with baseline TC and LDL-C and changes with training in LDL-C and TG entering into the model. A similar r2 was found for the change in LDL-C with baseline TC and LDL-C and changes in TC and HDL-C entering into the model. The r2 for change in TG was 0.473 with baseline body mass and the changes with training in body mass and TC entering into the model.

Table 5
Table 5
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DISCUSSION

Evidence evaluation.

Does the available evidence support the hypothesis that endurance exercise training has a favorable influence on the blood lipid profile relative to future risk of CHD? Although there is a great deal of inconsistency in the response of blood lipids to endurance exercise training in both RCT and non-RCT, the bulk of the evidence supports this hypothesis. The most frequently observed change is an increase in HDL-C, a protective factor against CHD (Evidence Category B). It is estimated that for every 0.026 mmol·L-1 (1 mg·dL-1) increase in HDL-C, the risk for a CHD event is reduced by 2% in men and at least 3% in women (51,52). Reduction in TC, LDL-C, and TG also may occur with training (Category B). In general, a 1% reduction in LDL-C is associated with a 2–3% lower risk of CHD (47). Exercise training also appears to attenuate the reduction in HDL-C accompanying a decreased dietary intake of saturated fat and cholesterol to promote reduction of LDL-C.

Does the blood lipid response to trainingdiffer by sex, age, race/ethnicity of study subjects, and baseline lipid levels, and baseline body weight and its change with training? Earlier reviewers noted a trend for a lower prevalence of training-induced increase in HDL-C levels in women (13,17,38,69). However, the data reviewed here suggest that sex is not a predictor of responsiveness of HDL-C to training, with adult men and women appearing to respond similarly (Category B). Age also does not appear to be a predictor of lipid responsiveness to exercise training, with elderly men and women as likely, or perhaps even more likely, than younger individuals to increase HDL-C with training (Category B). Only limited data are available on racial and ethnic differences in the response of lipids to exercise training. In the largest supervised exercise training study to date, the HERITAGE Family Study, there were no significant sex, age, or black/white differences in the extent (and variability) of the HDL-C response to training (43). Baseline body weight was found in this review to be inversely related to change in TG (but not to the other lipid variables under consideration). Studies in which a sizable weight loss was obtained while holding the percent of energy intake constant generally had a favorable effect on the entire lipid/lipoprotein profile (Category A); however, a concomitant reduction in percent energy from fat clearly reduces the HDL-C response to exercise. Only a limited number of studies have been performed on people with hypercholesterolemia and/or hypertriglyceridemia. On the basis of this review, baseline lipid levels appear to strongly influence the lipid response to training. A low pretraining HDL-C was shown to be a moderately strong predictor of a positive HDL-C response to training, whereas baseline LDL-C was inversely associated with posttraining change in TC (Category B).

Is the response of blood lipids to exercise related to the intensity, duration, the weekly volume of energy expenditure; the length of the endurance exercise program; and the associated change in V̇O2max? There currently are insufficient data from available training studies to conclusively establish a dose-response relationship between intensity and volume of exercise and lipid responses, suggested by observational studies (13,38,81). There have been only a limited number of studies directly evaluating the effects of different exercise intensities on blood lipids. Most of the studies reviewed here showing HDL-C changes used an exercise prescription involving moderate- to hard-intensity activities for at least 30 min, three times per week can raise HDL-C (Category B evidence for moderate- to hard-intensity exercise). There is limited evidence of additional benefits from higher intensity exercise (Category C). There also is limited evidence that lower intensity (light-intensity) exercise may be as effective as moderate-intensity exercise in raising HDL-C (Category C). No differences were found between HDL-C responders and nonresponders to training in the duration of exercise sessions and weekly volume of exercise performed. This probably was because the weekly volume of exercise used in most of the studies in this survey (a mean of about 6276 kJ (1500 kcal) for men and 5044 kg (1205 kcal) for women) probably exceeded the threshold required to increase HDL-C. In addition, no association was found between length of the training program (>12 wk) and HDL-C response (Category B). It also appears from the studies in Tables 1–3 that prescribed nonstructured or so-called lifestyle activities have little or no impact on the blood lipid profile (Category B). In most of the studies reported here, training resulted in at least a moderate increase in V̇O2max, as would be expected, since investigators generally followed ACSM exercise prescription guidelines for improving V̇O2max. However, no significant correlation was found between the increase in V̇O2max and change in HDL-C with training (Category A).

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Research priorities.

There remain many unanswered questions pertaining to the impact of exercise on blood lipids and lipoprotein that require future studies. Subjects for future investigations should include ethnic minorities and people of all ages with dyslipidemia, including those with isolated low HDL-C levels, since there is currently a paucity of data from such populations. Recommended study topics should include:

1. Large-scale, multicenter RCT to better define the dose-response relationships of progressively higher weekly volumes of energy expenditure via light-, moderate-, and hard-intensity exercise on blood lipid responses for periods up to 1 yr, with repeated lipid measurements during training to determine the relationship of duration of training to the observed lipid changes (e.g., measurements at 3, 6, 9, and 12 mo).

2. Investigations to determine how long exercise-induced changes persist during “detraining,” and to define the minimal or optimal volume of exercise to maintain exercise-induced lipid changes.

3. Investigations to better elucidate true training-induced blood lipid adaptations from transient (acute) effects of the most recent training session (e.g., by performing blood lipid assays adjusted for plasma volume changes at 12, 24, 48, and 72 h after the last training session).

4. Additional metabolic studies to better define mechanisms for blood lipid changes with exercise training.

5. Further investigations on the contribution of site-specific reductions in adipose tissue mass to blood lipid response to training.

6. Molecular biological investigations to identify genetic markers for HDL-C responders and nonresponders to exercise training.

7. Studies to further investigate the interactions of simultaneous dietary interventions and exercise training on blood lipids in patients with dyslipidemias with attempts to modify the diet plan so as to achieve optimal LDL-C reduction without adversely affecting the HDL-C (and TG) response to exercise.

8. Investigation of the interactions of cholesterol-lowering medications (particularly the HMG-coenzyme A reductase inhibitors or “statin” drugs) and exercise programs on blood lipids.

Thanks are expressed to Marilyn Borkon for preparation of this manuscript and to our graduate assistant, Sara Forbord, for help with data analysis and entry.

Dr. Arthur Leon is supported in part by the Henry L. Taylor Professorship in Exercise Science and Health Enhancement, The National Heart, Lung and Blood Institutes grant No. HL 47323, the American Heart Association (grant No. 9970017N), and by multiple pharmaceutical company research grants to the Heart Disease Prevention Clinic. Dr. Otto Sanchez is partially supported by Universidad de Oriente, Escuela de Medicina, Dpto de Ciencias Fisiologicas, Cd Bolivar, Edo Bolivar, Venezuela.

Address for correspondence: Arthur S. Leon, M.D., H.L. Taylor Professor, 202 Cooke Hall, Division of Kinesiology, University of Minnesota, 1900 University Avenue SE, Minneapolis, MN 55455; E-Mail: leonx002@tc.umn.edu.

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American Journal of Epidemiology
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Archives of Biological Sciences
Effects of Three Types of Physical Activity on Reduction of Metabolic Parameters Involved in Cardiovascular Risk
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Archives of Medical Science
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Southern Medical Journal
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Preventive Medicine
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Biochimica Et Biophysica Acta-Molecular and Cell Biology of Lipids
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International Journal of Sport Nutrition and Exercise Metabolism
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International Journal of Sport Nutrition and Exercise Metabolism, 15(4): 425-432.

European Journal of Applied Physiology
Body composition, fitness, and metabolic health during strength and endurance training and their combination in middle-aged and older women
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Biological Psychology
Increases in lipids and immune cells in response to exercise and mental stress in patients with suspected coronary artery disease: effects of adjustment for shifts in plasma volume
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Lipids in Health and Disease
Effects of cardiovascular lifestyle change on lipoprotein subclass profiles defined by nuclear magnetic resonance spectroscopy
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Preventive Medicine
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Metabolism-Clinical and Experimental
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Biological Research for Nursing
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Diabetes Care
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Sports Medicine
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Brain Behavior and Immunity
Effect of exercise training on C-reactive protein in postmenopausal breast cancer survivors: A randomized controlled trial
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Occupational Medicine-Oxford
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American Heart Journal
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American Journal of Physiology-Endocrinology and Metabolism
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International Journal of Obesity
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Progress in Neuro-Psychopharmacology & Biological Psychiatry
Low HDL cholesterol associates with major depression in a sample with a 7-year history of depressive symptoms
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Circulation
Associations of Physical Activity With Inflammatory Factors, Adipocytokines, and Metabolic Syndrome in Middle-Aged and Older Chinese People
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New England Journal of Medicine
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Arteriosclerosis Thrombosis and Vascular Biology
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Cancer Investigation
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Herz
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International Journal of Epidemiology
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International Journal of Obesity
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Cleveland Clinic Journal of Medicine
Why and how to prescribe exercise: Overcoming the barriers
Fletcher, G; Trejo, JF
Cleveland Clinic Journal of Medicine, 72(8): 645-+.

Annals of Medicine
The concept of cardiometabolic risk: Bridging the fields of diabetology and cardiology
Despres, JP; Cartier, A; Cote, M; Arsenault, BJ
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Metabolism-Clinical and Experimental
The effects of physical exercise on plasma prebeta-1 high-density lipoprotein
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Diabetes Care
High-intensity resistance training improves glycemic control in older patients with type 2 diabetes
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Science & Sports
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Nutrition Research
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Current Atherosclerosis Reports
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Journal of the American College of Nutrition
Reducing diet and/or exercise training decreases the lipid and lipoprotein risk factors of moderately obese women
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Scandinavian Journal of Medicine & Science in Sports
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Canadian Journal of Diabetes
A Pilot Study of Physical Activity Education Delivery in Diabetes Education Centres in Ontario
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Public Health Nutrition
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How Effective Is Exercise in Producing Fat Loss?
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Current Vascular Pharmacology
Current Management of Intermittent Claudication: The Role of Pharmacological and Nonpharmacological Symptom-Directed Therapies
Mangiafico, RA; Fiore, CE
Current Vascular Pharmacology, 7(3): 394-413.

Progress in Cardiovascular Diseases
Nonpharmacologic Treatment of Dyslipidemia
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Obesity
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Canadian Family Physician
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Acta Cardiologica
Physical exercise and coronary artery disease
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Sports Medicine
What is the relationship between exercise and metabolic abnormalities? A review of the metabolic syndrome
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Archives of Internal Medicine
Prescribing exercise at varied levels of intensity and frequency - A randomized trial
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British Journal of Sports Medicine
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Endocrinology and Metabolism Clinics of North America
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Scandinavian Journal of Medicine & Science in Sports
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Atherosclerosis
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New England Journal of Medicine
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Journal of Sports Medicine and Physical Fitness
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Applied Physiology Nutrition and Metabolism-Physiologie Appliquee Nutrition Et Metabolisme
Physical activity, cardiorespiratory fitness, and metabolic syndrome in young Mexican and Mexican-American women
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European Journal of Vascular and Endovascular Surgery
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Journal of Muscle Research and Cell Motility
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Medicina Clinica
Physical activity and cardiovascular and metabolic risk factors in general population
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Journal of Applied Physiology
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Medicine and Science in Sports and Exercise
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Canadian Journal of Applied Physiology-Revue Canadienne De Physiologie Appliquee
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European Journal of Applied Physiology
Nine months aerobic fitness induced changes on blood lipids and lipoproteins in untrained subjects versus controls
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European Journal of Epidemiology
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Annals of Nutrition and Metabolism
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Nutricion Hospitalaria
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Circulation
2012 ACCF/AHA/ACP/AATS/PCNA/SCAI/STS Guideline for the Diagnosis and Management of Patients With Stable Ischemic Heart Disease A Report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, and the American College of Physicians, American Association for Thoracic Surgery, Preventive Cardiovascular Nurses Association, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons
Fihn, SD; Gardin, JM; Abrams, J; Berra, K; Blankenship, JC; Dallas, AP; Douglas, PS; Foody, JM; Gerber, TC; Hinderliter, AL; King, SB; Kligfield, PD; Krumholz, HM; Kwong, RYK; Lim, MJ; Linderbaum, JA; Mack, MJ; Munger, MA; Prager, RL; Sabik, JF; Shaw, LJ; Sikkema, JD; Smith, CR; Smith, SC; Spertus, JA; Williams, SV
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Back to Top | Article Outline
Keywords:

EXERCISE; BLOOD LIPIDS; CHOLESTEROL; HDL; TRIGLYCERIDE

© 2001 Lippincott Williams & Wilkins, Inc.

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