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Effect of lower limb preference on local muscular and vascular function
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Institute of Physics and Engineering in Medicine
Physiological Measurement
doi:10.1088/0967-3334/35/1/83
Physiol. Meas. 35 (2014) 83–92
Effect of lower limb preference on local muscular and vascular function Christopher A Fahs 1,4 , Robert S Thiebaud 2 , Lindy M Rossow 1 , Jeremy P Loenneke 2 , Daeyeol Kim 2 , Takashi Abe 3 and Michael G Bemben 2 1
Department of Exercise and Sports Science, Fitchburg State University, Fitchburg, MA, USA 2 Department of Health and Exercise Science, University of Oklahoma, Norman, OK, USA 3 Department of Kinesiology, Indiana University, Bloomington, IN, USA E-mail: [email protected] Received 26 June 2013 Accepted for publication 8 November 2013 Published 17 December 2013 Abstract
Unilateral physical training can enhance muscular size and function as well as vascular function in the trained limb. In non-athletes, the preferred arm for use during unilateral tasks may exhibit greater muscular strength compared to the non-preferred arm. It is unclear if lower limb preference affects lower limb vascular function or muscular endurance and power in recreationally active adults. To examine the effect of lower limb preference on quadriceps muscle size and function and on lower limb vascular function in middle-aged adults. Twenty (13 men, 7 women) recreationally-active middle-aged (55 ± 7 yrs) adults underwent measurements of quadriceps muscle thickness, strength, mean power, endurance, and arterial stiffness, calf venous compliance, and calf blood flow in the preferred and non-preferred lower limb. The preferred limb exhibited greater calf vascular conductance (31.6 ± 15.5 versus 25.8 ± 13.0 units flow/mmHg; p = 0.011) compared to the non-preferred limb. The interlimb difference in calf vascular conductance was negatively related to weekly aerobic activity (hrs/week) (r = −0.521; p = 0.019). Lower limb preference affects calf blood flow but not quadriceps muscle size or function. Studies involving unilateral lower limb testing procedures in middle-aged individuals should consider standardizing the testing to either the preferred or non-preferred limb rather than the right or left limb. Keywords: arterial stiffness, venous compliance, blood flow, muscle endurance, muscle strength, muscle power 4
Author to whom any correspondence should be addressed.
0967-3334/14/010083+10$33.00
© 2014 Institute of Physics and Engineering in Medicine Printed in the UK
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1. Introduction Muscle size and function as well as vascular function (e.g. arterial stiffness, blood flow) measures are commonly used in both clinical and applied science studies. Often, assessments are made on one limb and the results are generalized to both limbs. Both muscle size and function and vascular function are affected by physical activity and the preferred limb (i.e. limb used for unilateral tasks) may exhibit enhanced muscle size, function, and or vascular function as a result of greater use. For example, post-exercise brachial artery blood flow (Kagaya et al 2010) and post-occlusive forearm blood flow and grip strength (Green et al 1996) are enhanced in the preferred (dominant) arm of tennis players. Additionally, radial artery distensibility is greater in the preferred arm of hammer throwers and baseball players (Giannattasio et al 2001). Even in non-athletes the preferred arm exhibits greater grip strength (Armstrong and Oldham 1999). While many studies have documented the effect of limb (hand) preference on forearm strength and blood flow in the upper limbs, only a few studies have documented a similar phenomenon in lower limb muscular strength. Isometric and isokinetic knee extensor strength are ∼5% greater in the preferred lower limb of females with physical activity patterns ranging from sedentary to very active (Hunter et al 2000, Lanshammar and Ribom 2011). In contrast, no effect of lower limb preference was observed on isokinetic strength in preadolescent boys (Burnie and Brodie 1986) or on unilateral squat strength in young healthy men and women (McCurdy and Langford 2005). It may be that the effect of limb preference on lower limb muscle strength may not be apparent until later in life as these changes may be due to slight differences in physical activity over the lifespan. Additionally, it is not clear if lower limb preference may affect local vascular function or other parameters of lower limb muscle function such as muscular power and endurance. Therefore, the purpose of this study was to examine the effect of lower limb preference on quadriceps muscle size and function and on arterial stiffness, calf venous compliance, and calf vascular conductance in recreationallyactive middle-aged adults. We hypothesized that middle-aged individuals would exhibit greater quadriceps muscle size and function, calf venous compliance, and calf vascular conductance and lower arterial stiffness in the preferred limb compared to the non-preferred limb. 2. Methods 2.1. Participants
Fourteen men and eight postmenopausal women aged 40–64 yrs were recruited to participate in this study. All participants provided written informed consent to participate, this study was approved by the University’s Institutional Review Board, and conformed with the guiding principles of research involving human beings. One man was excluded because of orthopedic problems preventing strength testing and one woman dropped out after the initial screening visit. Included participants (N = 20; 13 men, 7 women) did not smoke, did not have any orthopedic problems preventing strength testing, were not currently resistance training (or had not resistance trained within the last six months), had a brachial BP 140/90 mmHg, had an ankle-brachial index (ABI) 0.90, and were free of overt disease as assessed by a health history questionnaire (table 1). None of the participants reported any previous knee injuries and none of the postmenopausal women were taking hormone replacement therapy at the time of the study. Five participants were taking cholesterol lowering medication, four participants were taking blood pressure lowering medication, and two participants were taking thyroid medication. 84
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Table 1. Participant characteristics (N = 20). Data presented as mean (SD); BMI, body mass index; BP, blood pressure; MAP, mean arterial pressure; ABI, ankle-brachial index.
Age (yrs) Height (m) Body mass (kg) BMI (kg m−2) Systolic BP (mmHg) Diastolic BP (mmHg) MAP (mmHg) ABI Aerobic activity (hrs/week) Preferred limb (right/left) Cholesterol lowering medication (no.) BP lowering medication (no.) Thyroid medication (no.)
55 (7) 1.75 (0.10) 83.0 (15.7) 27.0 (4.6) 121 (13) 77 (9) 91 (11) 1.1 (0.1) 2.5 (2.0) 17/3 5 4 2
2.2. Study design
Participants visited the laboratory for a screening visit during which ABI was assessed to screen for peripheral vascular disease. Following this visit, participants returned for a familiarization visit and then a testing session in which measures of arterial stiffness, calf blood flow (CBF), calf venous compliance, thigh circumference, and quadriceps muscle thickness, strength, power, and endurance were obtained (in order) on each limb. Leg preference was determined by asking the participant which leg they would prefer to use for unilateral tasks (e.g. kicking a ball). For reliability purposes, participants returned to the laboratory for a second testing visit approximately three weeks later during which all measurements were repeated; all participants except for one man completed this visit. Participants were instructed to avoid caffeine (minimum 4 h), food (minimum 3 h), anti-inflammatory drugs (minimum 24 h), and strenuous activity (minimum 24 h) before both testing visits and both visits took place at the same time of day. If participants were taking any antioxidants, they were instructed to take it on both testing visits.
2.3. Screening visit
During this visit participants first filled out a health history questionnaire which included an assessment of the number of hours per week they engaged in any form of aerobic activity. Participants were asked ‘Do you regularly engage in aerobic (such as running, walking, biking, swimming) exercise? If you answered ‘yes’, how frequently (hours per week) have you engaged in aerobic activities during the past six months?’ For the ABI measurement, a vascular cuff was placed on each upper arm 2–3 cm above the antecubital space and on each leg 1–2 cm above the malleolus and the cuff was inflated with a manual handheld cuff inflator. To detect arterial blood flow, a Doppler probe (MD6 Bidirectional Doppler, DE Hokanson Inc., Bellevue, WA) was placed distal to the vascular cuff, over the brachial artery for brachial measurements and over the posterior tibial artery for ankle measurements. The vascular cuff was inflated to a pressure above that at which arterial blood flow could be detected and was then slowly deflated (2–3 mm Hg s−1). The highest pressure at which arterial flow could be detected during deflation was recorded as the systolic pressure in each limb. ABI was calculated as the lower ankle pressure divided by the higher brachial pressure. 85
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2.4. Familiarization visit
The knee extensor machine (NT 1220, Nautilus, Louisville, CO, USA) was adjusted for the participant and these settings were recorded for the subsequent testing sessions. Participants were instructed on the strength and power testing procedures, practiced the tests with submaximal loads, and also practiced performing the knee extensor exercise to the cadence of the metronome. 2.5. Testing visits
Following a minimum of 10 min of quiet supine rest, brachial systolic and diastolic blood pressure were measured using an automatic blood pressure measuring device (Omron Healthcare Inc., Vernon Hills, IL) on the left arm. Two measurements were taken 1 min apart and averaged. If these measurements were not with 5 mmHg, a third measurement was taken and the closest two values were averaged and used for analysis. Mean arterial pressure (MAP) was calculated using the formula: MAP = (2/3)DBP + (1/3)SBP. Femoral-tibial pulse wave velocity (PWV) was measured in accordance with current guidelines (Van Bortel et al 2002). The distance from the femoral artery pulse to the posterior tibial artery pulse was measured as a straight line with a tape measure. Using a high-fidelity strain-gauge transducer (SphygmoCor, AtCor Medical, Sydney, Australia), pressure waveforms were obtained at each pulse location. During the measurement, an electrocardiogram (ECG) was recorded to obtain heart rate and was used as a timing marker. Femoral-tibial PWV was calculated from the distance between measurement points and the measured time delay between the proximal (femoral) and distal (posterior tibial) waveforms relative to the peak of the R-wave recorded from the ECG and expressed as meters per second (m s−1). Calf venous compliance was assessed with strain gauge plethysmography (Sumner 1993). Both legs were elevated (14 cm) above heart level and an appropriately-sized venous collecting cuff was placed on each thigh (4–5 cm above patella) and an appropriately-sized strain gauge (2–3 cm smaller than the maximum circumference of the calf) connected to the plethysmograph was placed around each calf at the point of maximum circumference. The venous collecting cuff was inflated to 20 mmHg for 45 s, followed by subsequent cuff inflation pressures of 20, 40, 60, and 80 mmHg which were sustained for 1, 2, 3, and 4 min, respectively, with 1 min allotted between inflations to allow for baseline reestablishment and to prevent edema (Bleeker et al 2004). Venous volume variation (VVV; ml/100 ml) was defined as the maximal volume change in the calf at each cuff pressure and recorded by the plethysmograph in the Noninvasive Vascular Program (NIVP3, D.E. Hokanson Inc., Bellevue, WA). VVV was plotted across cuff pressures (20, 40, 60, 80 mmHg) to create a pressure–volume curve. Calf venous compliance (ml/100ml/mmHg) was calculated from the slope of the pressure–volume curve. CBF measurements were also obtained using strain gauge plethysmography. The participant’s legs remained in the same position and the setup was the same as described for the calf venous compliance measurement. The venous collecting cuff was inflated to 50 mmHg for 7 s while the plethysmograph recorded the arterial inflow. Every inflation was followed by an 8 s deflation. Six measurements were taken on each leg and averaged for analysis. Calf vascular conductance was calculated as flow per unit pressure (mmHg) using the formula: calf vascular conductance = (CBF/MAP) ∗ 1000. 86
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Thigh circumference was measured with a tape measure at 50% of the distance between the lateral epicondyle of the femur and the greater trochanter with the participant supine and the legs passively elevated. B-mode ultrasound was used to measure quadriceps muscle thickness (MTh) (Abe et al 1997). Measurements were obtained on the lateral (LT) and anterior (AT) surface of the thigh at 50% of the distance between the lateral epicondyle of the femur and the greater trochanter. Distances between bony landmarks were measured with a tape measure and marked with a pen. All ultrasound measurements were made using a Fukuda Denshi UF-750XT (Tokyo, Japan) ultrasound unit and a linear probe with a frequency of 6 MHz and the depth and gain adjusted to optimize the image. The probe was coated with transmission gel and placed perpendicular to the tissue surface at the marked sites without depressing the skin. MTh was determined as the distance from the adipose tissue–muscle interface to the muscle–bone interface and measured on-screen with electronic calipers to the nearest 0.01 cm. Two measurements of MTh at each site were obtained and averaged. All muscle thickness measurements were taken with the participant standing with their legs fully extended. For quadriceps strength, the maximum load that could be lifted through a full range of motion with proper form during unilateral knee extension was assessed and recorded as the one-repetition maximum (1RM). For each limb, the 1RM was assessed following standard 1RM procedures (Harman et al 2000). Muscular power was assessed during unilateral knee extension at three relative loads (30%, 60%, and 90% 1RM). The loads used to assess power were relative to the 1RM measured during that same visit. The participant was instructed to complete the concentric portion of the repetition as fast as possible. Two trials were completed at each load, in ascending order, and separated by a minimum of 1 min rest. A TENDO Fitrodyne Sports Powerlyzer unit was attached to the arm connecting the shin pad to the load which measured the mean velocity (m s–1) during each trial. For each load, the greater of the two mean velocities was used for analysis. Mean power (watts) was calculated using the formula (Harman et al 2000): Mean power (watts) = [load (kg) × mean velocity (m/s)]/0.10197. Following the muscular power test, the participant was given a minimum of 3 min rest. The load was adjusted to 30% 1RM measured on that visit. Participants completed one set of unilateral knee extension exercise to volitional fatigue at a pace of 20 repetitions per minute. The number of repetitions completed through a full range of motion was recorded as a measure of muscular endurance. 2.6. Statistical analyses
All data were analyzed using PASW Statistics 18 (Chicago, IL, USA). All data are expressed as mean ± standard deviation (SD). All dependent variables were tested for normality with the Shapiro–Wilk test. Paired samples differences for normally distributed variables were analyzed with Student’s t-tests whereas non-normally distributed variables were analyzed with the Wilcoxon test. Pearson correlations were used to examine the relationship between aerobic activity and the interlimb difference in quadriceps muscle and function and vascular function. For all statistical tests, an alpha level of 0.05 was used. Reliability (intraclass correlation coefficient, ICC3,1) for all dependent variables was calculated from the two testing sessions and the standard error of the measurement (SEM3,1) was calculated using the following equation (Weir 2005): √ SEM = SD 1 − ICC. 87
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Figure 1. Correlation between the interlimb difference (preferred limb − non-preferred limb) in calf vascular conductance and self-reported aerobic activity.
Coefficient of variation (%CV) was also calculated using the following formula: SD error %CV = . grand mean To determine the magnitude of the effect of limb preference on each dependent variable, the effect size (ES) was calculated using the following formula (Rhea 2004): (mean 1 − mean 2) . ES = SD 1
3. Results Muscular and vascular function variables are presented in table 2. The preferred limb exhibited greater calf vascular conductance (p = 0.011, ES = 0.037) than the non-preferred limb. The preferred limb also exhibited a tendency for greater calf venous compliance (p = 0.054; ES = 0.27) and PWV (p = 0.095; ES = 0.45) but these differences did not reach statistical significance. Aerobic activity was negatively related (p = 0.019; r = −0.521) to the interlimb difference in calf vascular conductance (figure 1). Individual interlimb differences (preferred − non-preferred limb) for select variables are presented in figures 2(a)–(d). 4. Discussion This study found that, in recreationally-active middle-aged individuals calf vascular conductance is greater in the preferred limb. The interlimb difference in calf vascular conductance was negatively related to the amount of aerobic activity performed per week. This suggests that performing aerobic activity may minimize the effect of lower limb preference on calf vascular conductance. Additionally, although not statistically significant, the preferred lower limb also exhibited greater arterial stiffness (femoral-tibial PWV) and venous compliance; the effect of limb preference on arterial stiffness and venous compliance was of a similar magnitude to that of the ES for limb preference on calf vascular conductance. Interlimb differences were not apparent for quadriceps muscle size or function. These results suggest 88
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(a)
(b)
(c)
(d)
Figure 2. (a)–(d). Interlimb differences (preferred limb − non-preferred limb) in
(a) PWV, (b) calf vascular conductance, (c) calf venous compliance, and (d) quadriceps muscle endurance. Dashed lines represent SEM. Positive values indicate preferred limb greater than non-preferred limb; negative value indicates preferred limb less than nonpreferred limb. Table 2. Muscular and vascular variables compared between limbs. Data presented as mean (SD); 1RM, one-repetition maximum; PWV, pulse wave velocity; AT, anterior thigh, LT, lateral thigh; MTh, muscle thickness; %CV, coefficient of variation; SEM, standard error of the measurement.
Strength (kg) 30% 1RM power (watts) 60% 1RM power (watts) 90% 1RM power (watts) Endurance (reps) PWV (m s−1) Calf vascular conductance (flow/mmHg) Venous compliance (ml/100ml/mmHg) Thigh circumference (cm) AT MTh (cm) LT MTh (cm)
Preferred
Non-preferred
P-value Effect size % CV SEM
27.0 (8.5) 79.9 (24.9) 128.9 (48.0) 141.3 (51.7) 32 (15) 9.3 (1.1) 31.6 (15.5)
27.0 (8.4) 78.1 (29.6) 124.1 (43.5) 138.1 (56.7) 28 (11) 8.8 (1.0) 25.8 (13.0)
1.000 0.633 0.213 0.585 0.968 0.095 0.011
0.00 0.07 0.10 0.06 0.36 0.45 0.37
7.10 11.38 10.60 8.81 17.00 5.83 29.12
0.0411 (0.0121) 0.0378 (0.0107) 0.054
0.27
17.98
53.5 (5.8) 5.28 (0.88) 3.54 (0.71)
0.05 0.01 0.03
2.07 4.69 3.26
53.2 (5.4) 5.27 (0.86) 3.52 (0.68)
89
0.550 0.893 0.749
2.4 12.7 16.7 17.7 8 0.7 11.1 0.0101 1.6 0.35 0.16
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that, in recreationally-active middle-aged individuals, limb preference influences lower limb vascular function but not quadriceps muscle size or function. Both knee extensor isometric (Hunter et al 2000) and isokinetic (Lanshammar and Ribom 2011) torque have been shown to be ∼5% greater in the preferred (dominant) leg. Our results suggest that there is no effect of leg preference on quadriceps isotonic strength. Although our findings appear contradictory to previous work, dynamic and isometric strength performance measures may be influenced by specific, rather than general, mechanisms (Baker et al 1994). In fact, other investigations observed no effect of leg preference (dominance) on unilateral squat strength in young adults (McCurdy and Langford 2005). Thus, based on our results and previous work, it appears that lower limb preference may influence isometric strength more than isotonic strength assessments. We also did not observe an effect of limb preference on mean power at either low, moderate, or high loads. This is likely because mean power is partially dependent on muscular strength as well as fiber type of the muscle. We hypothesized that the preferred limb would exhibit greater local muscular endurance potentially due to greater use during activities of daily living which require repeated submaximal quadriceps activation. Although there was no statistically different between limbs, quadriceps muscular endurance was greater in the preferred limb with 11 of the 20 participants exhibited greater endurance in the preferred limb and only three of the 20 participants exhibited greater endurance in the non-preferred limb (figure 2(d)). On average, the preferred limb was able to complete four more repetitions than the non-preferred limb but in four individuals this difference was 8 repetitions (exceeding the SEM). We did not observe an effect of limb preference on quadriceps muscle size. Thus, in recreationally active, middle-aged adults, limb preference does not influence quadriceps muscle size or function. The most notable finding of this study was the effect of limb preference on vascular function measures. Calf vascular conductance was greater in the preferred limb while both calf venous compliance and arterial stiffness tended to be greater in the preferred limb. On average, vascular conductance was 5.6 units flow/mmHg greater (∼22%) in the preferred limb compared to the non-preferred limb. Calf vascular conductance was greater in the preferred limb in the majority of individuals (15 of 20) and five individuals exhibited a substantial (exceeding the SEM) interlimb difference (>11 units flow/mmHg) in calf vascular conductance (figure 2(b)). To our knowledge this is the first study to investigate interlimb differences in basal blood flow of the lower limbs. Previous work has shown greater postexercise blood flow (Kagaya et al 2010) and post-occlusive blood flow (Green et al 1996) in the preferred forearm of tennis players. Our participants were only recreationally active and the interlimb difference in calf vascular conductance was inversely related to aerobic activity levels. Although not quantified, it is presumed that the activity reported involved both lower limbs which may explain why the interlimb difference in calf vascular conductance was lower in those individuals who were more active. Indeed, arterial lumen diameter both in the conduit and resistance vessels appears to be primarily influenced by local factors, mostly notably shear stress (Rowley et al 2011). Thus, it is likely that higher levels of physical activity may mitigate the effect of limb preference on CBF. The preferred lower limb also tended to exhibit greater arterial stiffness and calf venous compliance. Arterial stiffness, measured by PWV, was greater in the preferred limb in 12 of the 20 individuals and this difference was substantial (0.9 m s−1, exceeding the SEM) in five individuals (figure 2(a)). This finding was somewhat surprising as arterial distensibility has been shown to be higher in the preferred (dominant) limb of throwing athletes (Giannattasio et al 2001). To our knowledge this is the first study to investigate differences in lower limb arterial stiffness in non-athletes. PWV is related to the vessel wall to lumen ratio (Chirinos 2012). Thus, in middle aged individuals, the large arteries in the preferred limb may have an 90
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increased wall to lumen ratio although this finding should be confirmed by ultrasound imaging. Calf venous compliance was also greater in the preferred limb in 13 of the 20 participants but the difference was substantial (0.0100 ml/100ml/mmHg, exceeding the SEM) in just three individuals (figure 2(c)). We expected that the preferred limb would exhibit greater venous compliance because exercise training attenuates the age-related decline in calf venous compliance (Monahan et al 2001). Thus, our findings are in agreement with our hypothesis although the effect of limb preference appears to be rather modest on venous compliance. Differences in the structure of the venous wall and/or local factors that affect venous tone are the most likely mechanisms which would explain this difference. The reliability of quadriceps muscle size and function measurements ranged from acceptable to good. In contrast, the reliability for vascular measurements varied. PWV reliability was good (CV = 5.83%) whereas reliability for calf venous compliance (CV = 17.98%) and calf vascular conductance (CV = 29.12%) was acceptable and poor, respectively. Low reliability of basal CBF has been previously reported (Alomari et al 2004) and this occurs despite controlling for external factors (e.g. time of day, food intake, previous exercise) which may affect this measurement. Thus, this variability appears to be due mainly to biological variation. Based on the reliability for each outcome, we considered the interlimb difference to be substantial if the difference exceeded the SEM. A limitation of our study is that we have no measures of unilateral activity, past sports participation, or the type of aerobic activities our participants were currently performing at the time of the study (none of the participants engaged in resistance training). We also have no measure of calf muscle size or function which may explain some of the interlimb differences in calf vascular conductance and venous compliance. The use of plethysmography for the measurement of calf venous compliance does have limitations and some of the underlying assumptions (e.g. resting venous pressure is 0 mmHg) may be violated using this method (Halliwill et al 1999). Finally, we had a small sample of individuals with a left limb preference (3 of 20) although this proportion is similar to the frequency of left lower limb preference previously reported (∼5–10%) (Plato et al 1985).
5. Conclusions We observed that, in recreationally-active middle-aged adults, limb preference affects local vascular function but not quadriceps muscle size or function. The interlimb difference in calf vascular conductance may be minimized in physically active individuals as the difference is inversely related to the amount of aerobic activity performed. These interlimb differences observed in recreationally-active middle-aged adults are important as assessments of vascular function are often made on one limb and the results are generalized to both limbs. Studies involving unilateral lower limb testing procedures in middle-aged adults should consider standardizing the testing to either the preferred or non-preferred limb rather than the right or left limb.
Acknowledgments Supported by a grant for Doctoral Research in KAATSU Methodology from the American College of Sports Medicine (ACSM). 91
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Effect of lower limb preference on local muscular and vascular function
This content has been downloaded from IOPscience. Please scroll down to see the full text. 2014 Physiol. Meas. 35 83 (http://iopscience.iop.org/0967-3334/35/1/83) View the table of contents for this issue, or go to the journal homepage for more
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Please note that terms and conditions apply.
Institute of Physics and Engineering in Medicine
Physiological Measurement
doi:10.1088/0967-3334/35/1/83
Physiol. Meas. 35 (2014) 83–92
Effect of lower limb preference on local muscular and vascular function Christopher A Fahs 1,4 , Robert S Thiebaud 2 , Lindy M Rossow 1 , Jeremy P Loenneke 2 , Daeyeol Kim 2 , Takashi Abe 3 and Michael G Bemben 2 1
Department of Exercise and Sports Science, Fitchburg State University, Fitchburg, MA, USA 2 Department of Health and Exercise Science, University of Oklahoma, Norman, OK, USA 3 Department of Kinesiology, Indiana University, Bloomington, IN, USA E-mail: [email protected] Received 26 June 2013 Accepted for publication 8 November 2013 Published 17 December 2013 Abstract
Unilateral physical training can enhance muscular size and function as well as vascular function in the trained limb. In non-athletes, the preferred arm for use during unilateral tasks may exhibit greater muscular strength compared to the non-preferred arm. It is unclear if lower limb preference affects lower limb vascular function or muscular endurance and power in recreationally active adults. To examine the effect of lower limb preference on quadriceps muscle size and function and on lower limb vascular function in middle-aged adults. Twenty (13 men, 7 women) recreationally-active middle-aged (55 ± 7 yrs) adults underwent measurements of quadriceps muscle thickness, strength, mean power, endurance, and arterial stiffness, calf venous compliance, and calf blood flow in the preferred and non-preferred lower limb. The preferred limb exhibited greater calf vascular conductance (31.6 ± 15.5 versus 25.8 ± 13.0 units flow/mmHg; p = 0.011) compared to the non-preferred limb. The interlimb difference in calf vascular conductance was negatively related to weekly aerobic activity (hrs/week) (r = −0.521; p = 0.019). Lower limb preference affects calf blood flow but not quadriceps muscle size or function. Studies involving unilateral lower limb testing procedures in middle-aged individuals should consider standardizing the testing to either the preferred or non-preferred limb rather than the right or left limb. Keywords: arterial stiffness, venous compliance, blood flow, muscle endurance, muscle strength, muscle power 4
Author to whom any correspondence should be addressed.
0967-3334/14/010083+10$33.00
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1. Introduction Muscle size and function as well as vascular function (e.g. arterial stiffness, blood flow) measures are commonly used in both clinical and applied science studies. Often, assessments are made on one limb and the results are generalized to both limbs. Both muscle size and function and vascular function are affected by physical activity and the preferred limb (i.e. limb used for unilateral tasks) may exhibit enhanced muscle size, function, and or vascular function as a result of greater use. For example, post-exercise brachial artery blood flow (Kagaya et al 2010) and post-occlusive forearm blood flow and grip strength (Green et al 1996) are enhanced in the preferred (dominant) arm of tennis players. Additionally, radial artery distensibility is greater in the preferred arm of hammer throwers and baseball players (Giannattasio et al 2001). Even in non-athletes the preferred arm exhibits greater grip strength (Armstrong and Oldham 1999). While many studies have documented the effect of limb (hand) preference on forearm strength and blood flow in the upper limbs, only a few studies have documented a similar phenomenon in lower limb muscular strength. Isometric and isokinetic knee extensor strength are ∼5% greater in the preferred lower limb of females with physical activity patterns ranging from sedentary to very active (Hunter et al 2000, Lanshammar and Ribom 2011). In contrast, no effect of lower limb preference was observed on isokinetic strength in preadolescent boys (Burnie and Brodie 1986) or on unilateral squat strength in young healthy men and women (McCurdy and Langford 2005). It may be that the effect of limb preference on lower limb muscle strength may not be apparent until later in life as these changes may be due to slight differences in physical activity over the lifespan. Additionally, it is not clear if lower limb preference may affect local vascular function or other parameters of lower limb muscle function such as muscular power and endurance. Therefore, the purpose of this study was to examine the effect of lower limb preference on quadriceps muscle size and function and on arterial stiffness, calf venous compliance, and calf vascular conductance in recreationallyactive middle-aged adults. We hypothesized that middle-aged individuals would exhibit greater quadriceps muscle size and function, calf venous compliance, and calf vascular conductance and lower arterial stiffness in the preferred limb compared to the non-preferred limb. 2. Methods 2.1. Participants
Fourteen men and eight postmenopausal women aged 40–64 yrs were recruited to participate in this study. All participants provided written informed consent to participate, this study was approved by the University’s Institutional Review Board, and conformed with the guiding principles of research involving human beings. One man was excluded because of orthopedic problems preventing strength testing and one woman dropped out after the initial screening visit. Included participants (N = 20; 13 men, 7 women) did not smoke, did not have any orthopedic problems preventing strength testing, were not currently resistance training (or had not resistance trained within the last six months), had a brachial BP 140/90 mmHg, had an ankle-brachial index (ABI) 0.90, and were free of overt disease as assessed by a health history questionnaire (table 1). None of the participants reported any previous knee injuries and none of the postmenopausal women were taking hormone replacement therapy at the time of the study. Five participants were taking cholesterol lowering medication, four participants were taking blood pressure lowering medication, and two participants were taking thyroid medication. 84
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Table 1. Participant characteristics (N = 20). Data presented as mean (SD); BMI, body mass index; BP, blood pressure; MAP, mean arterial pressure; ABI, ankle-brachial index.
Age (yrs) Height (m) Body mass (kg) BMI (kg m−2) Systolic BP (mmHg) Diastolic BP (mmHg) MAP (mmHg) ABI Aerobic activity (hrs/week) Preferred limb (right/left) Cholesterol lowering medication (no.) BP lowering medication (no.) Thyroid medication (no.)
55 (7) 1.75 (0.10) 83.0 (15.7) 27.0 (4.6) 121 (13) 77 (9) 91 (11) 1.1 (0.1) 2.5 (2.0) 17/3 5 4 2
2.2. Study design
Participants visited the laboratory for a screening visit during which ABI was assessed to screen for peripheral vascular disease. Following this visit, participants returned for a familiarization visit and then a testing session in which measures of arterial stiffness, calf blood flow (CBF), calf venous compliance, thigh circumference, and quadriceps muscle thickness, strength, power, and endurance were obtained (in order) on each limb. Leg preference was determined by asking the participant which leg they would prefer to use for unilateral tasks (e.g. kicking a ball). For reliability purposes, participants returned to the laboratory for a second testing visit approximately three weeks later during which all measurements were repeated; all participants except for one man completed this visit. Participants were instructed to avoid caffeine (minimum 4 h), food (minimum 3 h), anti-inflammatory drugs (minimum 24 h), and strenuous activity (minimum 24 h) before both testing visits and both visits took place at the same time of day. If participants were taking any antioxidants, they were instructed to take it on both testing visits.
2.3. Screening visit
During this visit participants first filled out a health history questionnaire which included an assessment of the number of hours per week they engaged in any form of aerobic activity. Participants were asked ‘Do you regularly engage in aerobic (such as running, walking, biking, swimming) exercise? If you answered ‘yes’, how frequently (hours per week) have you engaged in aerobic activities during the past six months?’ For the ABI measurement, a vascular cuff was placed on each upper arm 2–3 cm above the antecubital space and on each leg 1–2 cm above the malleolus and the cuff was inflated with a manual handheld cuff inflator. To detect arterial blood flow, a Doppler probe (MD6 Bidirectional Doppler, DE Hokanson Inc., Bellevue, WA) was placed distal to the vascular cuff, over the brachial artery for brachial measurements and over the posterior tibial artery for ankle measurements. The vascular cuff was inflated to a pressure above that at which arterial blood flow could be detected and was then slowly deflated (2–3 mm Hg s−1). The highest pressure at which arterial flow could be detected during deflation was recorded as the systolic pressure in each limb. ABI was calculated as the lower ankle pressure divided by the higher brachial pressure. 85
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2.4. Familiarization visit
The knee extensor machine (NT 1220, Nautilus, Louisville, CO, USA) was adjusted for the participant and these settings were recorded for the subsequent testing sessions. Participants were instructed on the strength and power testing procedures, practiced the tests with submaximal loads, and also practiced performing the knee extensor exercise to the cadence of the metronome. 2.5. Testing visits
Following a minimum of 10 min of quiet supine rest, brachial systolic and diastolic blood pressure were measured using an automatic blood pressure measuring device (Omron Healthcare Inc., Vernon Hills, IL) on the left arm. Two measurements were taken 1 min apart and averaged. If these measurements were not with 5 mmHg, a third measurement was taken and the closest two values were averaged and used for analysis. Mean arterial pressure (MAP) was calculated using the formula: MAP = (2/3)DBP + (1/3)SBP. Femoral-tibial pulse wave velocity (PWV) was measured in accordance with current guidelines (Van Bortel et al 2002). The distance from the femoral artery pulse to the posterior tibial artery pulse was measured as a straight line with a tape measure. Using a high-fidelity strain-gauge transducer (SphygmoCor, AtCor Medical, Sydney, Australia), pressure waveforms were obtained at each pulse location. During the measurement, an electrocardiogram (ECG) was recorded to obtain heart rate and was used as a timing marker. Femoral-tibial PWV was calculated from the distance between measurement points and the measured time delay between the proximal (femoral) and distal (posterior tibial) waveforms relative to the peak of the R-wave recorded from the ECG and expressed as meters per second (m s−1). Calf venous compliance was assessed with strain gauge plethysmography (Sumner 1993). Both legs were elevated (14 cm) above heart level and an appropriately-sized venous collecting cuff was placed on each thigh (4–5 cm above patella) and an appropriately-sized strain gauge (2–3 cm smaller than the maximum circumference of the calf) connected to the plethysmograph was placed around each calf at the point of maximum circumference. The venous collecting cuff was inflated to 20 mmHg for 45 s, followed by subsequent cuff inflation pressures of 20, 40, 60, and 80 mmHg which were sustained for 1, 2, 3, and 4 min, respectively, with 1 min allotted between inflations to allow for baseline reestablishment and to prevent edema (Bleeker et al 2004). Venous volume variation (VVV; ml/100 ml) was defined as the maximal volume change in the calf at each cuff pressure and recorded by the plethysmograph in the Noninvasive Vascular Program (NIVP3, D.E. Hokanson Inc., Bellevue, WA). VVV was plotted across cuff pressures (20, 40, 60, 80 mmHg) to create a pressure–volume curve. Calf venous compliance (ml/100ml/mmHg) was calculated from the slope of the pressure–volume curve. CBF measurements were also obtained using strain gauge plethysmography. The participant’s legs remained in the same position and the setup was the same as described for the calf venous compliance measurement. The venous collecting cuff was inflated to 50 mmHg for 7 s while the plethysmograph recorded the arterial inflow. Every inflation was followed by an 8 s deflation. Six measurements were taken on each leg and averaged for analysis. Calf vascular conductance was calculated as flow per unit pressure (mmHg) using the formula: calf vascular conductance = (CBF/MAP) ∗ 1000. 86
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Thigh circumference was measured with a tape measure at 50% of the distance between the lateral epicondyle of the femur and the greater trochanter with the participant supine and the legs passively elevated. B-mode ultrasound was used to measure quadriceps muscle thickness (MTh) (Abe et al 1997). Measurements were obtained on the lateral (LT) and anterior (AT) surface of the thigh at 50% of the distance between the lateral epicondyle of the femur and the greater trochanter. Distances between bony landmarks were measured with a tape measure and marked with a pen. All ultrasound measurements were made using a Fukuda Denshi UF-750XT (Tokyo, Japan) ultrasound unit and a linear probe with a frequency of 6 MHz and the depth and gain adjusted to optimize the image. The probe was coated with transmission gel and placed perpendicular to the tissue surface at the marked sites without depressing the skin. MTh was determined as the distance from the adipose tissue–muscle interface to the muscle–bone interface and measured on-screen with electronic calipers to the nearest 0.01 cm. Two measurements of MTh at each site were obtained and averaged. All muscle thickness measurements were taken with the participant standing with their legs fully extended. For quadriceps strength, the maximum load that could be lifted through a full range of motion with proper form during unilateral knee extension was assessed and recorded as the one-repetition maximum (1RM). For each limb, the 1RM was assessed following standard 1RM procedures (Harman et al 2000). Muscular power was assessed during unilateral knee extension at three relative loads (30%, 60%, and 90% 1RM). The loads used to assess power were relative to the 1RM measured during that same visit. The participant was instructed to complete the concentric portion of the repetition as fast as possible. Two trials were completed at each load, in ascending order, and separated by a minimum of 1 min rest. A TENDO Fitrodyne Sports Powerlyzer unit was attached to the arm connecting the shin pad to the load which measured the mean velocity (m s–1) during each trial. For each load, the greater of the two mean velocities was used for analysis. Mean power (watts) was calculated using the formula (Harman et al 2000): Mean power (watts) = [load (kg) × mean velocity (m/s)]/0.10197. Following the muscular power test, the participant was given a minimum of 3 min rest. The load was adjusted to 30% 1RM measured on that visit. Participants completed one set of unilateral knee extension exercise to volitional fatigue at a pace of 20 repetitions per minute. The number of repetitions completed through a full range of motion was recorded as a measure of muscular endurance. 2.6. Statistical analyses
All data were analyzed using PASW Statistics 18 (Chicago, IL, USA). All data are expressed as mean ± standard deviation (SD). All dependent variables were tested for normality with the Shapiro–Wilk test. Paired samples differences for normally distributed variables were analyzed with Student’s t-tests whereas non-normally distributed variables were analyzed with the Wilcoxon test. Pearson correlations were used to examine the relationship between aerobic activity and the interlimb difference in quadriceps muscle and function and vascular function. For all statistical tests, an alpha level of 0.05 was used. Reliability (intraclass correlation coefficient, ICC3,1) for all dependent variables was calculated from the two testing sessions and the standard error of the measurement (SEM3,1) was calculated using the following equation (Weir 2005): √ SEM = SD 1 − ICC. 87
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Figure 1. Correlation between the interlimb difference (preferred limb − non-preferred limb) in calf vascular conductance and self-reported aerobic activity.
Coefficient of variation (%CV) was also calculated using the following formula: SD error %CV = . grand mean To determine the magnitude of the effect of limb preference on each dependent variable, the effect size (ES) was calculated using the following formula (Rhea 2004): (mean 1 − mean 2) . ES = SD 1
3. Results Muscular and vascular function variables are presented in table 2. The preferred limb exhibited greater calf vascular conductance (p = 0.011, ES = 0.037) than the non-preferred limb. The preferred limb also exhibited a tendency for greater calf venous compliance (p = 0.054; ES = 0.27) and PWV (p = 0.095; ES = 0.45) but these differences did not reach statistical significance. Aerobic activity was negatively related (p = 0.019; r = −0.521) to the interlimb difference in calf vascular conductance (figure 1). Individual interlimb differences (preferred − non-preferred limb) for select variables are presented in figures 2(a)–(d). 4. Discussion This study found that, in recreationally-active middle-aged individuals calf vascular conductance is greater in the preferred limb. The interlimb difference in calf vascular conductance was negatively related to the amount of aerobic activity performed per week. This suggests that performing aerobic activity may minimize the effect of lower limb preference on calf vascular conductance. Additionally, although not statistically significant, the preferred lower limb also exhibited greater arterial stiffness (femoral-tibial PWV) and venous compliance; the effect of limb preference on arterial stiffness and venous compliance was of a similar magnitude to that of the ES for limb preference on calf vascular conductance. Interlimb differences were not apparent for quadriceps muscle size or function. These results suggest 88
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(a)
(b)
(c)
(d)
Figure 2. (a)–(d). Interlimb differences (preferred limb − non-preferred limb) in
(a) PWV, (b) calf vascular conductance, (c) calf venous compliance, and (d) quadriceps muscle endurance. Dashed lines represent SEM. Positive values indicate preferred limb greater than non-preferred limb; negative value indicates preferred limb less than nonpreferred limb. Table 2. Muscular and vascular variables compared between limbs. Data presented as mean (SD); 1RM, one-repetition maximum; PWV, pulse wave velocity; AT, anterior thigh, LT, lateral thigh; MTh, muscle thickness; %CV, coefficient of variation; SEM, standard error of the measurement.
Strength (kg) 30% 1RM power (watts) 60% 1RM power (watts) 90% 1RM power (watts) Endurance (reps) PWV (m s−1) Calf vascular conductance (flow/mmHg) Venous compliance (ml/100ml/mmHg) Thigh circumference (cm) AT MTh (cm) LT MTh (cm)
Preferred
Non-preferred
P-value Effect size % CV SEM
27.0 (8.5) 79.9 (24.9) 128.9 (48.0) 141.3 (51.7) 32 (15) 9.3 (1.1) 31.6 (15.5)
27.0 (8.4) 78.1 (29.6) 124.1 (43.5) 138.1 (56.7) 28 (11) 8.8 (1.0) 25.8 (13.0)
1.000 0.633 0.213 0.585 0.968 0.095 0.011
0.00 0.07 0.10 0.06 0.36 0.45 0.37
7.10 11.38 10.60 8.81 17.00 5.83 29.12
0.0411 (0.0121) 0.0378 (0.0107) 0.054
0.27
17.98
53.5 (5.8) 5.28 (0.88) 3.54 (0.71)
0.05 0.01 0.03
2.07 4.69 3.26
53.2 (5.4) 5.27 (0.86) 3.52 (0.68)
89
0.550 0.893 0.749
2.4 12.7 16.7 17.7 8 0.7 11.1 0.0101 1.6 0.35 0.16
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that, in recreationally-active middle-aged individuals, limb preference influences lower limb vascular function but not quadriceps muscle size or function. Both knee extensor isometric (Hunter et al 2000) and isokinetic (Lanshammar and Ribom 2011) torque have been shown to be ∼5% greater in the preferred (dominant) leg. Our results suggest that there is no effect of leg preference on quadriceps isotonic strength. Although our findings appear contradictory to previous work, dynamic and isometric strength performance measures may be influenced by specific, rather than general, mechanisms (Baker et al 1994). In fact, other investigations observed no effect of leg preference (dominance) on unilateral squat strength in young adults (McCurdy and Langford 2005). Thus, based on our results and previous work, it appears that lower limb preference may influence isometric strength more than isotonic strength assessments. We also did not observe an effect of limb preference on mean power at either low, moderate, or high loads. This is likely because mean power is partially dependent on muscular strength as well as fiber type of the muscle. We hypothesized that the preferred limb would exhibit greater local muscular endurance potentially due to greater use during activities of daily living which require repeated submaximal quadriceps activation. Although there was no statistically different between limbs, quadriceps muscular endurance was greater in the preferred limb with 11 of the 20 participants exhibited greater endurance in the preferred limb and only three of the 20 participants exhibited greater endurance in the non-preferred limb (figure 2(d)). On average, the preferred limb was able to complete four more repetitions than the non-preferred limb but in four individuals this difference was 8 repetitions (exceeding the SEM). We did not observe an effect of limb preference on quadriceps muscle size. Thus, in recreationally active, middle-aged adults, limb preference does not influence quadriceps muscle size or function. The most notable finding of this study was the effect of limb preference on vascular function measures. Calf vascular conductance was greater in the preferred limb while both calf venous compliance and arterial stiffness tended to be greater in the preferred limb. On average, vascular conductance was 5.6 units flow/mmHg greater (∼22%) in the preferred limb compared to the non-preferred limb. Calf vascular conductance was greater in the preferred limb in the majority of individuals (15 of 20) and five individuals exhibited a substantial (exceeding the SEM) interlimb difference (>11 units flow/mmHg) in calf vascular conductance (figure 2(b)). To our knowledge this is the first study to investigate interlimb differences in basal blood flow of the lower limbs. Previous work has shown greater postexercise blood flow (Kagaya et al 2010) and post-occlusive blood flow (Green et al 1996) in the preferred forearm of tennis players. Our participants were only recreationally active and the interlimb difference in calf vascular conductance was inversely related to aerobic activity levels. Although not quantified, it is presumed that the activity reported involved both lower limbs which may explain why the interlimb difference in calf vascular conductance was lower in those individuals who were more active. Indeed, arterial lumen diameter both in the conduit and resistance vessels appears to be primarily influenced by local factors, mostly notably shear stress (Rowley et al 2011). Thus, it is likely that higher levels of physical activity may mitigate the effect of limb preference on CBF. The preferred lower limb also tended to exhibit greater arterial stiffness and calf venous compliance. Arterial stiffness, measured by PWV, was greater in the preferred limb in 12 of the 20 individuals and this difference was substantial (0.9 m s−1, exceeding the SEM) in five individuals (figure 2(a)). This finding was somewhat surprising as arterial distensibility has been shown to be higher in the preferred (dominant) limb of throwing athletes (Giannattasio et al 2001). To our knowledge this is the first study to investigate differences in lower limb arterial stiffness in non-athletes. PWV is related to the vessel wall to lumen ratio (Chirinos 2012). Thus, in middle aged individuals, the large arteries in the preferred limb may have an 90
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increased wall to lumen ratio although this finding should be confirmed by ultrasound imaging. Calf venous compliance was also greater in the preferred limb in 13 of the 20 participants but the difference was substantial (0.0100 ml/100ml/mmHg, exceeding the SEM) in just three individuals (figure 2(c)). We expected that the preferred limb would exhibit greater venous compliance because exercise training attenuates the age-related decline in calf venous compliance (Monahan et al 2001). Thus, our findings are in agreement with our hypothesis although the effect of limb preference appears to be rather modest on venous compliance. Differences in the structure of the venous wall and/or local factors that affect venous tone are the most likely mechanisms which would explain this difference. The reliability of quadriceps muscle size and function measurements ranged from acceptable to good. In contrast, the reliability for vascular measurements varied. PWV reliability was good (CV = 5.83%) whereas reliability for calf venous compliance (CV = 17.98%) and calf vascular conductance (CV = 29.12%) was acceptable and poor, respectively. Low reliability of basal CBF has been previously reported (Alomari et al 2004) and this occurs despite controlling for external factors (e.g. time of day, food intake, previous exercise) which may affect this measurement. Thus, this variability appears to be due mainly to biological variation. Based on the reliability for each outcome, we considered the interlimb difference to be substantial if the difference exceeded the SEM. A limitation of our study is that we have no measures of unilateral activity, past sports participation, or the type of aerobic activities our participants were currently performing at the time of the study (none of the participants engaged in resistance training). We also have no measure of calf muscle size or function which may explain some of the interlimb differences in calf vascular conductance and venous compliance. The use of plethysmography for the measurement of calf venous compliance does have limitations and some of the underlying assumptions (e.g. resting venous pressure is 0 mmHg) may be violated using this method (Halliwill et al 1999). Finally, we had a small sample of individuals with a left limb preference (3 of 20) although this proportion is similar to the frequency of left lower limb preference previously reported (∼5–10%) (Plato et al 1985).
5. Conclusions We observed that, in recreationally-active middle-aged adults, limb preference affects local vascular function but not quadriceps muscle size or function. The interlimb difference in calf vascular conductance may be minimized in physically active individuals as the difference is inversely related to the amount of aerobic activity performed. These interlimb differences observed in recreationally-active middle-aged adults are important as assessments of vascular function are often made on one limb and the results are generalized to both limbs. Studies involving unilateral lower limb testing procedures in middle-aged adults should consider standardizing the testing to either the preferred or non-preferred limb rather than the right or left limb.
Acknowledgments Supported by a grant for Doctoral Research in KAATSU Methodology from the American College of Sports Medicine (ACSM). 91
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