Effects on blood lipids and body weight in high risk men of a practical exercise program

Atherosclerosis, 49 (1983) 219-229 Elsevi:r Scientific Publishers Ireland.

219 Ltd

ATH 03402

Effects on Blood Lipids and Body Weight in High Risk Men of a Practical Exercise Program George Sopko, David R. Jacobs, Jr., Robert Jeffery, Maurice Mittelmark, Kristine Lenz, Elizabeth Hedding, Randy Lipchik and Wendy Gerber Laboratory of Physiological Hygiene, School of Public Health. Universrt_~ of Minnesota. 55455 (U.S.A.)

Mmneapolis.

MN

(Received 8 October, 1982) (Accepted 22 June, 1983)

Summary The effects of moderate exercise on serum total cholesterol (TC), high density (HDL-C), low density (LDL-C), and very low density (VLDL-C) lipoprotein cholesterol fractions, triglycerides (TG), body weight (BW) and skinfolds (SF) were studied during a 12-week period among 23 sedentary middle-aged men. The results show that regular exercise in men eating a fat-modified diet alters in a favorable direction body fat, weight and lipoprotein fractions. Weight loss with exercise significantly increased HDL-C (P = O.Ol), although this increase in HDL-C occurred after a latency period of at least 6 weeks and an average weight loss of at least 4 lbs. The amount of exercise effective in risk factor reduction is within the capacity of most middle-aged men. Key words:

Exercise

- Lipoprotein

fractions

~ Serum lipids

Introduction Elevated serum cholesterol is positively related to coronary heart disease (CHD) risk in individuals as well as whole populations [1,2]. Epidemiologic and experimen-

Supported in part by a grant from the School of Public Health, University of Minnesota (GRS 100695225), by NHBLI (NOlHV2-2976C). and by a Research Career Development Award to Dr. Jacobs (HL-00287). Address for reprints: George Sopko M.D., M.P.H., Department of Medicine, University of Mihnesota, Minneapolis, MN 55455, U.S.A.

OOZl-9150/83/$03.00

0 1983 Elsevier Scientific

Publishers

Ireland,

Ltd.

220

tal studies indicate that LDL-C is the fraction directly related and HDL-C inversely related to the CHD risk [3,4]. Individual TC levels are determined by genetic and environmental factors. Diet and exercise have the most significant environmental roles. Exercise modifies serum lipid levels, possibly through the mechanism of weight reduction [5]. The effect of moderate exercise and its interaction with weight in men eating a fat-modified diet on serum lipids and body composition is examined here. Methods and Materials Subjects The subjects are middle-aged men who have participated for the past 4 years in the NHBLI sponsored Multiple Risk Factor Intervention Trial (MRFIT), a randomized clinical trial of primary CHD prevention [6]. The men have been followed at the Laboratory of Physiological Hygiene (LPH), School of Public Health, University of Minnesota. All were counselled in a specific eating pattern designed to lower dietary cholesterol, total caloric intake and fat (especially saturated fat) to achieve TC reduction. The men in the special intervention group, who had not achieved their “goal TC or BW level” formed the study group. A randomized controlled design was not permitted within MRFIT protocol. However, the opportunity to study effects of moderate exercise in a quasi-controlled study was afforded by a MRFIT subprogram designed to create long-term trial participation and to learn how to change the life habits of men in the greatest need. Out of two hundred eligible men contacted by a letter and return postcard, the first 69 (31%) responders were accepted. Twenty seven (14%) indicated interest in the to take part. Their ages ranged from 43 to 60 yrs study and 23 (12%) consented (mean 53.6 yrs). Inclusion criteria for this intervention were: BW > 20% of recommended, and/or TC > 220 mg/lOO ml. Ten subjects chose the combined Diet/ Exercise program and 13 chose the the Diet only program. Both programs aimed toward gradual and sustained weight reduction based on the MRFIT dietary recommendations. Both groups started simultaneously and were followed for 12 weeks. All subjects were sedentary and none smoked. Four subjects in the Diet group and 6 subjects in the Diet/Exercise group remained on antihypertensive (diuretic) therapy throughout the study. Anthropometric data Height and weight were measured with a calibrated standard medical scale in shorts and socks. Three SF measurements were taken at each triceps and subscapular sites with Lange calipers and a standard protocol. Blood pressure was recorded according to the MRFIT protocol with a random zero muddler and correct size cuff at the beginning and end of the study. Lipoprotein determination The blood for TC, TG and lipoproteins was collected from all on 2 consecutive days at baseline, 6 and 12 weeks. Average values were used in analysis. The collection was made after fasting 6 h and after working hours to minimize subject’s

221

economic loss. It preserved uniformity. TC and TG were determined with the Technicon Autoanalyser II technique according to LRC Laboratory Manual [7]. Lipoproteins were determined by combined ultracentrifugal and heparin/ manganese method [7] at the Central Lipid Laboratory for MRFIT. Exercise program The 12-week program consisted of l-h sessions of walking on a treadmill 3 times a week (Monday, Wednesday, Friday). The prescribed caloric expenditure, 400-500 kcal per session, represents a ‘socially acceptable’ exercise level for individuals who are changing from sedentary to active status. All 23 men were screened for contraindications to exercise and all were capable of exercising. Workload increased within the first 2 weeks and was kept stable thereafter, an average of 3 mph at 4% grade, not exceeding 5% grade elevation or 3.5 mph speed. A physician supervised all sessions, Pre- and post-exercise HR and BW were routinely recorded. The ECG was not monitored. Individual and average session energy cost were calculated [8]; the group average was 420 kcal per session. The attendance was 79% (range 43-98%). Out of town travel was the main reason for absence. Two subjects dropped out at 6 weeks, one moved out of the area and another’s business schedule interfered. Their attendance was 75% and 61%. respectively. Diet program The program consisted of counselling sessions held for each group on alternate weeks with the instructors and session content identical for both groups. The program was based on the MRFIT Progressive Eating Pattern (PEP) composition: lowering dietary cholesterol to 100 mg/day and total fat to 25% of daily caloric intake, 5% from saturated (SAFA) and 10% from polyunsaturated (PUFA) fat. The targeted food patterns were: (1) reduced total fat intake with partial substitution of PUFA for SAFA; (2) decreased red meat consumption and increased meatless alternatives; (3) care in eating away from home. Three-day food records, collected at baseline, 6 and 12 weeks, provided information about current eating patterns. The records were checked by the staff and men were familiar with the recording method. Educational efforts promoted skill development to change eating habits emphasizing gradual, specific dietary changes. Wives were encouraged to attend and their attendance, at least once, was 67% for the Diet/Exercise and 54% for the Diet group. Respective participant’s group attendance was 85% and 77% (range 50-100% for both groups). Dietary data were analyzed with a computer dietary analysis program developed at LPH and based on USDA Handbook 8. Furthermore, using MRFIT group categories a daily total score (FRR) was calculated for each fat-containing food groups [9]. The dietary changes at 6 and 12 weeks were expressed as percent change from baseline. Statistics Analysis was made using BMDP [lo] programs on a PDP 11 computer. Hypothasis tests employed an ANOVA, for specific variables a paired t-test for the group’s

1

197.5 * 74.0

Two sample paired r-tests of the hypothesis * P = 0.06: *** P = 0.01.

Triglycerides

38.1 f 11.8

Very low density lipoproteins

7.8

45.6*

High density lipoproteins

163.0 + 22.4

Low density lipoproteins

k137.0

20.9

6.3 *

18.4

21.6

Standard

in change

6.1

1.2

5.2

7.1

between

-8.O+

8.8

1.2

1.5

9.0

groups.

111.7 treatment

78.8+

7.1*

-1.8+

-14.3*

D

error of the change

(n = 10 IN DE AND n = 12

3.8 *

2.0 ***

8.3

8.4

to 12 weeks

0.6&

-0.5*

-6.7+

-5.8+

4.3

1.5

6.8

7.7

- 25.9 + 23.4

D

is given for 6 weeks and 12 weeks.

- 62.6 k 25.4

- 11.2+

5.4*

-4.3+

- 10.4+

DE

Baseline

from baseline

(n = 10 IN DE AND n = 13 IN D), 6 WEEKS

to 6 weeks

-40.2+35.3

-6.9+

-i.7*

-13.6+

-18.4+

that there is no difference

249

44.1+

36.0+

156.0&

235.0 +

D

DE

242.8 * 25.0

Total cholesterol

DE

is given for baseline.

Baseline

in each group

AT BASELINE

Baseline

Standard deviation for each measurement Measurements are in mg/dl.

MEAN FOR DIET/EXERCISE (DE) AND DIET (D) GROUPS IN D) AND 12 WEEKS (n = 9 IN DE AND n = 12 IN D)

TABLE

2

deviation

122.2 f 24.7

190.4 + 30.6

that there is no difference

138.8 f 39.8

195.4 * 34.9

in change

_

-4.3t1.3

between

***

groups.

_

0.2+ 1.1

D

error of the change

Baseline to 6 weeks

Standard

DE

D

is given for baseline.

DE

in each group

Baseline

for each measurement

Two sample paired r-tests of the hypothesis * P = 0.06; ** P = 0.04; *** P = 0.01.

(mm)

Sum of skin folds

Body weight (Ibs.)

Standard

AT BASELINE

(n = 10 IN

**

to 12 weeks

-1.8k1.4

~ 11 .o * 4.9

D

is given for 6 weeks and 12 weeks.

- 21.1 * 3.2 *

-7.lk2.1

DE

Baseline

from baseline

MEAN BODY WEIGHT AND SUM OF 6 SKIN FOLD VALUES FOR DIET/EXERCISE (DE) AND DIET (D) GROUPS DE AND n = 13 IN D), 6 WEEKS (n = 10 IN DE AND n = 12 IN D) AND 12 WEEKS (n = 9 IN DE AND n = 12 IN D)

TABLE

224

differences and a two-sample paired t-test for differences between treatment groups were used. The relationship between serum lipids and other variables was assessed by linear regression method. The significance level was assessed at 1%.

Results Analysis of pre-study variables showed significantly higher HDL-C levels in the seeTable 1. The differences between the groups Diet/Exercise group (P = 0.04), were tested for all variables and unless specified otherwise they were insignificant. A statistically marginal decrease of 1.7 mg/dl (P = 0.06) in HDL-C was observed at 6 weeks in each group. HDL-C significantly increased by 5.4 mg/dl from baseline to 12 weeks in the Diet/Exercise group (P = 0.01); an increase was noted in all but one man. The Diet group showed insignificant HDL-C change; there was a decrease in 8 men and an increase in 4 men. VLDL-C decreased from baseline to 12 weeks by 11.2 mg/dl in the Diet/Exercise group (again in all but one man) as compared to an increase of 0.6 mg/dl in the Diet group (P = 0.06). TG decreased from baseline to 12 weeks in both groups but this decrease did not differ significantly between the groups. In both groups, increases in HDL-C tended to be accompanied by decreases in VLDL-C and TG. LDL-C and TC both decreased by 6 weeks in each group, with some return toward the baseline levels by 12 weeks. Between group differences were not statistically significant, however. Table 2 shows the Diet/Exercise group’s weight loss throughout the study (4.3 lbs at 6 weeks and 7.1 lbs at 12 weeks). This weight loss was significantly greater in the Diet/Exercise group than in the Diet group. Table 3 shows greater HDL-C change in men who lost over 6 lbs than those who lost less (P = 0.08). The sum of SF from both sites decreased from baseline to 12 weeks. The decrease was marginally greater in the Diet/Exercise than in the Diet group.

TABLE

3

MEAN AND STANDARD ERROR FOR CHANGE IN WEIGHT AND HDL CHOLESTEROL, AND FOR CALORIC EXPENDITURE (TREADMILL/EXERCISE PROGRAM) FOR DIET/ EXERCISE GROUP PARTICIPANTS FROM BASELINE TO 12 WEEKS Weight loss (Ibs.)

Total caloric expenditure

HDL-C (mg/dI)

observed

All men (n = 9)

8.8 *1.5

10851 *1041

5.4 * 2.0

Men with weight loss t 6 lbs. (n = 4)

13.2 +0.8

12821 * 814

8.1 + 2.5

Men with weight loss 5 6 Ibs. (n = 5)

5.3 * 0.5

9 762 k1762

3.3 f 2.6

changes

225

TABLE

4

TOTAL CALORIC (DE) (n = 9) AND

INTAKE AND DIET COMPOSITION DIET GROUP (n = 12) AT BASELINE

FOR MEN IN DIET/EXERCISE

GROUP

The dietary components are expressed in means and SD, as a percent of total caloric intake. Standard error and the mean percent change from baseline is given for 12 weeks (n = 8 in DE and n = 12 in D). Baseline to 12 weeks

Baseline

Intake (K Cal/day Total fat (%) Cholesterol (mg/lOO Protein (W) Carbohydrate (8) FRR score

ml)

DE

D

DE

D

1725 ?332 34.4+ 6.4 283.4* 130.3 19.4* 3.5 44.0* 9.9 11.2+ 7.6

1501 +418 33.3* 8.1 238.9 + 95.8 19.8* 5.6 47.5* 8.8 9.3+ 2.5

0.3 * 10.1 -5.3+14.8 - 70.0 + 56.3 -8.Ok 5.7 16.2 * 16.3 -1.5+ 2.0

8.1 + 8.2 22.4 k 27.9 -45.8~46.1 0.5j, 7.6 16.5 + 13.1 -1.6+ 1.4

Both changes within and differences between the Diet/Exercise and Diet groups in caloric, carbohydrate or total fat consumption were insignificant, see Table 4. At baseline 21% (SD 35.3) and 4.4% of calories (SD 5.8) came from alcohol in Diet/Exercise and Diet group, respectively. Alcohol intake increased within the first 6 weeks from 25.5 g (SE 80.7) to 41.4 g (SE 23.2) for Diet/Exercise group and from 9.8 g (SE 12.3) to 69.4 g (SE 57.8) for Diet group. The increase from baseline to 12 weeks was 26.8 g (SE 22.3) and 34.3 g (SE 25.9). These changes were insignificaht and most likely reflect daily variations in food-alcohol intake. The relationship between alcohol intake and change in HDL-C was also insignificant. Changes Ln food categories, such as baked goods, dairy products and eggs were insignificant. Resting HR decreased in the Diet/Exercise group by 10.5 beats/min (SE 3.7) from baseline to 12 weeks (P = 0.04). Discussion The study shows a biphasic HDL-C response with initially no change or a marginal decrease followed by a significant increase. This HDL-C increase from, 6 weeks to 12 was accompanied by a decrease in VLDL-C, and noted only in the Diet/Exercise group. It was preceded by a continuous weight loss in the Diet/ Exercise group throughout the study. There is some suggestion that amount of HDL-C increase by 12 weeks is greater for greater weight loss. However, it should be borne in mind that this weight loss was the result of exercise, not decrease in caloric intake. Weight loss through dietary restriction may not have the same effect on HDL-C as weight loss through increased energy expenditure. Though TC, LDL-C and TG were measured in this study, and all decreased somewhat more in the Diet/Exercise group than in the Diet group, the study had insufficient power for calling such decreases statistically significant. Given the observed within person variation in these variates, a study with at least 5 times ‘as many subjects in each group would be required to detect statistically significant decreases of magnitude actually observed.

226

The intervention prior to this ‘subproject’ had changed the participants’ eating patterns. As a group they met the larger MRFIT dietary goals, This is reflected by the FRR score shown in Table 4. A score I 9 indicates adherence to basic MRFIT dietary recommendations (300 mg cholesterol/day, with I 8% of total calories from SAFA and 10% from PUFA). A score I 4 indicates adherence to the PEP program. Thus, these men were eating a fat modified diet, but did not achieved the dietary goal of the PEP program. Since the PEP intervention was designed primarily to promote long-term gradual changes, the short 12-week study period may have allowed insufficient time for change. In view of the exposure to specific dietary instructions over the past 4 years prior to this study, it is not surprising that only slight alterations in eating pattern occurred in this study. The reported caloric intake for both groups was 400-600 kcal/day lower than expected for men of their age [II]. Neither group showed a significant change in dietary variables during the study. Though apparent underreporting of calories throws suspicion on the validity of the initial levels of dietary variables, the relative lack of a change in TC and BW in the Diet group tends to support the accuracy of these dietary change data. This lack of dietary change is actually an asset in the interpretation of exercise-related effects in this study, since this removes one potentially confounding variable between the Diet/Exercise and Diet group. The non-randomized design required by the MRFIT protocol limits interpretation of these data. To compensate for the study design several quasi-control features were used. Each man served as his own control and the Diet group served as a concurrent time control for the Diet/Exercise group. Dietary instructions and practices in both groups were similar. Possible effect of self-selection is noted in subjects who chose the exercise program; they had higher baseline HDL-C levels. Similar findings were noted in the study by Williams et al. [12], where higher HDL-C levels were observed in the subjects with a tendency toward higher physical activity level. This raises the possibility that these individuals have an easier time exercising than those who choose not to exercise. However, even if this choice is somehow biologically determined, the fact that people who prefer to exercise can raise HDL-C is of practical significance. Interest in physical activity and its ability to modify CHD risk factors dates back to late 1950’s. Several epidemiological studies found lower CHD mortality in subjects with higher levels of physical activity [13-161. These beneficial effects of physical activity may be mediated in part through exercise-induced serum lipid changes. Cross-sectional data show that physically active subjects have significantly higher HDL-C and lower LDL-C than inactive subjects [17-221. Though exercise training affects serum TC variably [23-261, in males HDL-C level usually increases [27-331. This increase was apparent if the training exceeded 7 weeks and two studies reported significant correlation between the study length and HDL-C change [12,28]. Weight loss was observed in some but not all studies. It is known that HDL-C levels are inversely related to relative weight [1,21]. In women, active weight loss alone has been reported to (temporarily) decrease HDL-C levels [34,35], but the former study [34] was of of short duration and therefore not

227

inconsistent with our findings. In the latter study [35] HDL-C increased after weight was stabilized at lower level. Experience from this laboratory [5] showed that 16 weeks of daily rigorous exercise accompanied with weight loss increased HDL-C level, though 8 weeks did not. On the other hand, 8 or less weeks of exercise without weight loss neither changed nor decreased HDL-C significantly [36,37]. Therefore, the frequency, duration and intensity of exercise needed to significantly increase HDL-C remains yet to be determined. The possibility remains that HDL-C response to weight loss from exercise differs between men and women, young and old, obese and non-obese. Studies of the effects of exercise on HDL-C in obese subjects have yielded contrasting results [38,39]. That younger subjects may respond differently from older is suggested by several studies showing no significant difference in HDL-C levels between athletes and controls [27,28,40,41]. Our study excludes the possibility that the initial, transient reduction of HDLC in the exercising group seen here and in other studies [27,42] is due to the stress of beginning an exercise program, for nearly identical transient reductions were also seen in our non-exercising men. We conclude that weight loss as a result of exercise is followed after a period of latency or after a weight loss threshold is crossed by HDL-C increase. We can make no statements from these data about the effect on HDL-C of weight loss without exercise or exercise without weight loss. Therefore, the length of a study and the amount of weight loss, among other factors. could ‘be responsible for the reported discrepancies in exercise-related HDL-C changes. The clinical significance of these findings is based upon the assumption that raised HDL-C is an index of reduced individual risk for CHD in high-risk populations. The study provides a rational strategy for preventive practice in men at high risk for the development of premature CHD. It also suggests that regular exercise affects blood lipid levels, though weight loss probably facilitates the response. Furthermore, it appears that this moderate and practical type of exercise can also modify body composition and body weight and thus be used effectively in the management of obesity. References 1 Avogaro, P., Cazzolato, G., Bittolo Bon G. et al., HDL-cholesterol. apolipoproteins A and B, age and body index weight, Atherosclerosis, 31 (1978) 85. 2 Truett, J., Cornfield, J. and Kannel, W.B., A multivariety analysis of the risk of coronary disease in Framingham, J. Chron. Dis., 20 (1967) 511. 3 Miller, N., Rhoads, G.G., Gulbrandsen, C.L. and Kagan, A., Serum lipoprotein and heart disease in a population of Hawaii Japanese men, N. Engl. J. Med., 294 (1976) 293. 4 Nikkila, E., Studies on the lipid-protein relationships in normal and pathologic sera and the effect of heparin on serum lipoproteins, Stand. J. Clin. Lab. Invest., 5 (Suppl. 8) (1953) 1. 5 Leon, A.S., Conrad, J., Hunninghake, D.B. et al., Effects of walking program on body composition and carbohydrate and lipid metabolism of obese young men, Amer. J. Clin. Nutr.. 32 (1979) 1776. 6 Multiple risk factor intervention trial. Risk factor changes and mortality results, J. Amer. Med. Ass., 248 (1982) 1465. 7 Lipid and lipoprotein analysis. Lipid Research Clinic Manual of Laboratory Operations, Vol. 1, Dept. of Health, Education and Welfare publication (NIH), Government Printing Office, Washington, DC, 1974. p. 75-628.

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34 Thompson, lipoprotein

P.D.,

Jeffery,

cholesterol

R.W.,

Wing,

R.R.

et al., Unexpected

with weight loss, Amer. J. Clin. Nutr.,

decrease

in plasma

high density

32 (1979) 2016.

35 Friedman, CL, Falko, J.M., Patel, S.T. et al., Serum lipoprotein responses during active and stable weight reduction in reproductive obese females, J. Clin. Endocr. Metab., 55 (1982) 258. 36 Lipson, L.C., Bonow, R.O., Schaeffer, E.J. et al., Effect of exercise conditioning on plasma high density and other lipoproteins, Atherosclerosis, 37 (1980) 529. 37 Allison. T.G.. Iammarino, R.M., Metz, K.F. et al.. Failure of exercise to increase high density lipoprotein cholesterol, J. Card. Rehab., 4 (1981) 257. 38 Lewis. S., Haskell, W.L., Wood, P.D. et al., Effect of physical activity on weight reduction in obese middle aged women, Amer. J. Clin. Nutr., 29 (1976) 151. 39 Weltman, A., Malter, Sh. and Stamford, B.A., Caloric restriction and/or mild exercise .- Effect on serum lipids and body composition, Amer. J. Clin. Nutr., 33 (1980) 1002. 40 Marniemi, J., Dahlstrom, S., Krist, M. et al., Dependance of serum lipid and lecithin:cholesterol acyltransferase levels on physical training in young men, Europ. J. Appl. Physiol.. 37 (1982) 25. 41 Horby-Petersen, J., Grande, P. and Christiansen, C., Effect of physical training on serum lipids and serum HDL cholesterol in young men, Stand. J. Clin. Lab. Invest.. 42 (1982) 387. 42 Ferrell. P.A. and Barboriak, J., The time course of alterations in plasma lipid and lipoprotem concentrations during eight weeks of endurance training, Atherosclerosis, 37 (1980) 23.