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J Appl Physiol 101: 1351-1355, 2006. First published July 13, 2006; doi:10.1152/japplphysiol.00497.2006
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Resistance training increases basal limb blood flow and vascular conductance in aging humans

Maria M. Anton, Miriam Y. Cortez-Cooper, Allison E. DeVan, Daria B. Neidre, Jill N. Cook, and Hirofumi Tanaka

Department of Kinesiology and Health Education, University of Texas at Austin, Austin, Texas

Submitted 1 May 2006 ; accepted in final form 6 July 2006


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Age-related reductions in basal limb blood flow and vascular conductance are associated with the metabolic syndrome, functional impairments, and osteoporosis. We tested the hypothesis that a strength training program would increase basal femoral blood flow in aging adults. Twenty-six sedentary but healthy middle-aged and older subjects were randomly assigned to either a whole body strength training intervention group (52 ± 2 yr, 3 men, 10 women) who underwent three supervised resistance training sessions per week for 13 wk or a control group (53 ± 2 yr, 4 men, 9 women) who participated in a supervised stretching program. At baseline, there were no significant differences in blood pressure, cardiac output, basal femoral blood flow (via Doppler ultrasound), vascular conductance, and vascular resistance between the two groups. The strength training group increased maximal strength in all the major muscle groups tested (P < 0.05). Whole body lean body mass increased (P < 0.05) with strength training, but leg fat-free mass did not. Basal femoral blood flow and vascular conductance increased by 55–60% after strength training (both P < 0.05). No such changes were observed in the control group. In both groups, there were no significant changes in brachial blood pressure, plasma endothelin-1 and angiotensin II concentrations, femoral artery wall thickness, cardiac output, and systemic vascular resistance. Our results indicate that short-term strength training increases basal femoral blood flow and vascular conductance in healthy middle-aged and older adults.

vascular resistance; strength exercise; ultrasonics; hemodynamics

BASAL LIMB BLOOD FLOW AND vascular conductance decrease with advancing age even in healthy adults (2, 3, 16). Reductions in limb perfusion have been implicated in the pathogenesis of the metabolic syndrome (1, 10), which could contribute to the development of cardiovascular disease. Considering that reductions in limb blood flow and vascular conductance have important clinical and functional implications for aging adults, the search for effective strategies to prevent the age-related decline in this function is of paramount importance.

Regular exercise is an established intervention and treatment for the primary and secondary prevention of cardiovascular disease (12, 19), and it would appear to be a promising intervention to prevent age-related diminishment of limb perfusion. However, daily aerobic exercise was unable to attenuate or prevent the age-related reductions in basal limb blood flow and vascular conductance (4). In recent years, resistance training has become a critical component in exercise prescription programs for healthy adults (19, 20). As an initial step to address the relation between resistance training and basal limb blood flow, we performed a cross-sectional study and found that the decrease in limb blood flow was absent in middle-aged men who habitually performed resistance training (15). It was reasonable to hypothesize that a greater basal leg blood flow may be due to a larger skeletal muscle mass and the greater metabolic demands in resistance-trained men because both leg oxygen consumption and fat-free mass are strongly associated with whole leg blood flow (2–4). However, when blood flow was expressed relative to leg muscle mass, the results remained essentially the same (15). These results suggest that not only quantitative but also qualitative changes in skeletal muscle and/or alterations in nonskeletal muscle components induced by resistance training may be responsible for an absence of the age-related reduction in basal leg blood flow in resistance-trained men. Given the encouraging results from the cross-sectional study and the inherent limitations of cross-sectional comparisons, we reasoned that confirmation of these observations with an intervention study design was needed.

Accordingly, the primary aim of the present study was to determine the effects of strength training intervention on basal limb blood flow and vascular conductance in previously sedentary middle-aged and older adults. We hypothesized that a strength training program would increase basal limb perfusion. To account for the possibility of random changes over time in key outcome variables as well as the "attention" that the resistance training subjects would receive from their frequent visits to the laboratory and interactions with the investigative team, a group that performed supervised stretching exercises was used as an attention control group (11).


   METHODS
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 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
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Subjects

A total of 26 healthy middle-aged and older subjects (7 men, 19 women) were studied. All subjects were nonobese (body mass index <30 kg/m2), nonsmoking, normotensive (blood pressure <140/90 mmHg), normolipidemic, normoglycemic, and free of overt cardiovascular and other chronic diseases as assessed by medical questionnaire and physical examination. Older subjects (men over the age of 45 yr and women over the age of 55 yr) underwent a treadmill stress test to maximal exertion to screen for the presence of overt coronary heart disease. Subjects were not taking any cardiovascular acting medications, including hormone replacement therapy. None of the subjects had participated in any resistance or endurance training on a regular basis for the past year. Candidates who had significant intima-media thickening (IMT), plaque formation, and/or a sign of peripheral artery disease (ankle-brachial index <0.9) were excluded. All procedures were approved by the Institutional Review Board at The University of Texas at Austin, and written informed consent was obtained from each subject before participation. Subjects were subsequently randomized into either the strength intervention group or the attention control group that participated in supervised stretching sessions. Three women in each group were premenopausal, and they were studied during the early follicular phase of their menstrual cycle.

Procedures

All measurements were performed with the subjects in the supine position after a 12-h overnight fast and abstinence from caffeine and alcohol. All the testing was conducted under comfortable laboratory conditions early in the morning, and the time of the day that the experiments were conducted was not different between the groups. Subjects were studied at least 24 h after their last exercise session to avoid any acute effects of exercise while still being representative of their normal physiological state (i.e., habitually exercising).

Femoral artery hemodynamics.   A multifrequency probe attached to an ultrasound machine (model HDI-5000, Philips Bothel, WA) was used to measure common femoral artery mean blood velocity and arterial lumen diameter as previously described (2, 15). Measurements were performed ~2–3 cm proximal to the bifurcation of internal and external femoral arteries to minimize turbulence from the bifurcation. The insonation angle was ≤60°. Arterial lumen diameter was defined as the distance between the media-adventitia interface of the near wall and the lumen-intima interface of the far-wall of the vessel. Ultrasound images were transferred to digital viewing software (Access Point 2000, Freeland, Westfield, IN) where pulsatile changes in femoral artery diameter were analyzed. A mean diameter [D = D(systole/3) + D(diastole 2/3)] based on the relative time periods of the systolic () and diastolic () blood pressure phases was used to represent the cross-sectional area. Femoral blood flow was calculated as: MBV x {pi} x (femoral arterial radius)2 x 60, where MBV is mean blood velocity in centimeters per second, and 60 is used to convert from milliliters per second to milliliters per minute.

Blood pressure was measured in duplicate using an automatic oscillometric device (Colin Medical Instruments, San Antonio, TX). Femoral vascular conductance was calculated as femoral blood flow/mean arterial blood pressure, and femoral vascular resistance was calculated as mean arterial blood pressure/femoral blood flow. To eliminate interinvestigator variability, all image acquisition and image analyses were performed by the same investigator, who was blinded to the group assignment of the subjects.

Femoral artery IMT.   Femoral artery IMT was measured from images derived from an ultrasound machine equipped with a high-resolution linear-array transducer (model HDI-5000, Philips) as previously described (27). Ultrasound images were analyzed by use of computerized software (QLab, Phillips). The same investigator, who was blinded to the group assignment of subjects, performed all image analyses.

Cardiac output.   Stroke volume was measured by M-mode echocardiography (model HDI-5000, Phillips) equipped with a 2.5-MHz sector transducer. Cardiac output was calculated as the product of stroke volume and heart rate. Systemic vascular resistance was calculated as mean arterial blood pressure divided by cardiac output. All image acquisition and image analyses were performed by the same investigator, who was blinded to the group assignment of the subjects.

Body composition.   Body composition was determined by dual-energy X-ray absorptiometry (Lunar DPX, GE Medical Systems, Fairfield, CT). Leg fat-free mass was obtained from whole body scans as previously described (2).

Blood analyses.   After 12 h of fasting and 24 h of minimum physical activity, a blood sample was drawn from the antecubital vein for enzymatic determinations of plasma concentrations of glucose, lipid, and lipoproteins (Vitros DT60 analyzer, Ortho-Clinical Diagnostics, Raritan, NJ). Plasma norepinephrine (Labor Diagnostika Nord, Nordhorn, Germany) and plasma endothelin-1 concentrations (R&D Systems, Minneapolis, MN) were measured by enzyme immunoassay. Plasma angiotensin II concentrations (ALPCO Diagnostics, Windham, NH) were measured by radioimmunoassay.

Interventions.   Subjects in the strength training group underwent three supervised resistance training sessions per week for 13 wk. Maximal muscle strength was assessed by using one-repetition maximum (1 RM) strength tests during the second week and the conclusion of training. During each training session, the subjects completed a warm-up set at 50% 1 RM, and one primary set at 75% 1 RM. Subjects performed as many repetitions as possible to concentric failure in the primary set. Each training session included seated chest press, bilateral leg press, upper back, hamstrings, shoulders, triceps, biceps, calves, and abdominals. Resistance was increased for the following sessions when subjects were able to complete at least 12 repetitions in the primary set. Recovery time between exercises was controlled at 2-min intervals. A trained researcher verbally encouraged the subjects and ensured proper form and technique. Subjects in the attention control group underwent two supervised and one home-based stretching exercise sessions per week for 13 wk. The control group was constructed to control for the possibility of random changes in the key outcome variables as well as the attention that the exercise intervention group would receive from the investigators.

Statistics

Group differences in the dependent variables were assessed by mixed-model ANOVA. All data are reported as means ± SE. A significance level of P < 0.05 was used to determine statistical significance. When a significant interaction was observed, pairwise comparisons were made.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Before the intervention period, there were no significant differences in any of the variables between the two groups. Subjects in the intervention group completed over 90% of the scheduled training sessions. During the 13-wk training period, maximal muscle strength increased 30% in seated chest press, 30% in bilateral leg press, 26% in upper back, 34% in hamstrings, 33% in shoulders, 27% in triceps, and 35% in biceps (all P < 0.05). Because of the potential risks involved in maximal strength testing, these tests were not performed in the control group.

As shown in Table 1, there were no significant changes in body mass, body mass index, or percent body fat in either group. Whole body lean body mass increased (P < 0.05) with the strength training intervention, whereas no significant change was observed in leg fat-free mass. In both groups, there were no significant changes in fasting plasma concentrations of glucose, lipid, lipoproteins, endothelin-1, or angiotensin II (Table 2). Plasma norepinephrine concentrations increased (P < 0.05) after strength training. Brachial blood pressure, femoral artery IMT, cardiac output, and systemic vascular resistance did not change in either group (Table 3).


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  		Table 1. Selected subjects characteristics

 

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  		Table 2. Metabolic risk factors and hormone concentrations

 

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  		Table 3. Systemic and femoral hemodynamic characteristics

 
At baseline, there were no significant differences in femoral blood flow and femoral vascular conductance between the two groups. As illustrated in Figs. 1 and 2, basal femoral blood flow increased by ~60% (P < 0.05) after 13 wk of strength training. This was associated with a 56% increase in femoral vascular conductance and a 78% reduction in femoral vascular resistance (both P < 0.05; Fig. 1). The increase in femoral blood flow was primarily due to an increase in mean blood velocity because there was no change in lumen diameter. No significant changes in basal femoral blood flow, vascular conductance, and vascular resistance were observed in the control group. The changes in femoral blood flow or vascular conductance were not significantly associated with the changes in muscular strength (P = 0.29–0.38).


Figure 1
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  		Fig. 1. Mean (±SE) changes in basal femoral blood flow (top), vascular conductance (middle), and vascular resistance (bottom) in attention control and strength training groups. *P < 0.05 vs. Before.

 

Figure 2
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  		Fig. 2. Intraindividual changes in basal femoral blood flow (top), vascular conductance (middle), and vascular resistance (bottom) in attention control and strength training groups. *P < 0.05 vs. Before.

 

   DISCUSSION
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The present intervention study is the first to document the effects of resistance exercise training on basal limb blood flow and vascular conductance in healthy aging men and women. The major new findings are that basal femoral blood flow and vascular conductance increased significantly after 13 wk of strength training in previously sedentary middle-aged and older adults. The augmented basal femoral blood flow in the intervention group was not associated with leg muscle mass or systemic blood flow because they did not change significantly with exercise training. The present findings indicate that resistance training may be an effective strategy for the secondary treatment of age-related reductions in basal limb perfusion.

We have previously reported that middle-aged men performing resistance training on a regular basis demonstrated higher whole leg blood flow and vascular conductance than their sedentary peers (15). The present intervention study confirms these cross-sectional observations by demonstrating that a short-term strength training program increases basal femoral blood flow and vascular conductance in previously sedentary middle-aged and older adults. The present results are consistent with previous findings in patients with chronic heart failure in whom basal forearm blood flow increased after a moderate-intensity resistance training program (7, 25). Taken together, these results support the notion that habitual resistance exercise is associated with favorable effects on basal limb perfusion.

It is not clear what physiological mechanisms explain the increases in femoral blood flow with strength training. Because of the close coupling between blood flow and metabolically active tissue (i.e., muscle mass) and the well-documented effects of resistance training on muscle mass (5, 6), we hypothesized that resistance training would augment basal femoral blood flow by increasing leg muscle mass. However, leg muscle mass did not increase after strength training, although whole body fat-free mass did. This would suggest a possibility of changes in some qualitative (i.e., vasoactive), rather than quantitative (i.e., muscle mass oriented), properties in skeletal muscle and/or alterations in nonskeletal muscle components affecting basal femoral blood flow (8). In this context, tonically elevated sympathetic adrenergic vasoconstrictor tone has been suggested as a mechanism underlying age-related reductions in basal limb blood flow and vascular conductance (2). Given this, increases in femoral blood flow and vascular conductance might be due to reduced vasoconstriction activity. However, we observed an increase, rather than a decrease, in plasma concentration of norepinephrine, similar to other studies demonstrating associations between resistance training and increased sympathetic nervous system activity (21, 22). Additionally, there were no changes in plasma concentrations of potent vasoconstrictors, endothelin-1 and angiotensin II, after strength training. Recently, an intervention study involving young healthy men reported that strength training increased peak limb vasodilatory capacity (23), a surrogate measure of resistance artery structure (26). These results raise the possibility that enhanced vascular function at the arteriolar level may somehow contribute to the increased basal femoral blood flow and vascular conductance after strength training. Other possibilities include increases in nitric oxide bioavailability (18) and decreased myogenic tone (17). Obviously, further studies are warranted to investigate the physiological mechanisms underlying the effects of resistance training on basal femoral blood flow.

Our findings have important clinical implications. Reduced basal leg blood flow in peripheral tissues is associated with a reduction in the clearance of lipoproteins (10). Additionally, chronic reductions in basal limb blood flow and vascular conductance have been associated with reduced muscle glucose uptake and contribute to insulin resistance in middle-aged and older adults (1). Our present results suggest that the effects of weight training on basal limb perfusion may be a potential mechanism underlying previously observed effects of strength training on glucose uptake (20). As insulin resistance is a hallmark feature of the metabolic syndrome that could contribute to increased incidence of cardiovascular disease, strength training may confer another health benefits beyond the well-established impact on muscular strength and osteoporosis (9, 20). It should, however, be noted that strength training has been associated with the stiffening of large arteries in young and middle-aged adults (13, 14). Thus resistance training may have to be prescribed carefully based on the preexisting condition of subjects and the anticipated outcome of the exercise program.

In conclusion, the results of the present study indicate that 13 wk of strength training exercise can restore and attenuate the age-related reductions in basal femoral blood flow and vascular conductance. Chronic resistance training may be an effective lifestyle intervention for minimizing the reductions in limb blood flow with advancing age and improving perfusion.


   GRANTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
The present study was supported by National Institutes of Health (NIH) Award AG-20966. M. M. Anton, M. Y. Cortez-Cooper, and A. E. DeVan were supported by fellowship awards from the government of Spain and by NIH Grants HL-072729 and DA-018431.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
We thank Rhea Montemayor, Chris Mobley, Seth Holwerda, Phil Stanforth, and Jill Tanaka for assistance.


   FOOTNOTES
 

Address for reprint requests and other correspondence: H. Tanaka, Dept. of Kinesiology and Health Education, Univ. of Texas at Austin, Austin, TX 78712 (e-mail: htanaka{at}mail.utexas.edu)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 

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