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Page 1: Blood Pressure Responses To Small And Large Muscle Dynamic Exercise In Older Adults Of Different Aerobic Fitness Level

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Blood Pressure Responses to Small and Large Muscle Dynamic

Exercise in Older Adults of Different Aerobic Fitness Level

Dustin M. Grinnell, Joaquin U. Gonzales, and David N. Proctor*

Noll Laboratory, Department of Kinesiology, Pennsylvania State University, University Park, PA

*Corresponding Author:

David N. Proctor, Ph.D.

Associate Professor of Kinesiology, Physiology and Medicine

105 Noll Laboratory, The Pennsylvania State University

University Park, PA 16802

Phone: 814-863-0724 Fax: 814-865-4602

Email: [email protected]

Study funded in part from NIH grant R01 AG018246 to D.N. Proctor.

Running Head: Pressor responses, active muscle mass, and aging

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ABSTRACT

The aim of this study was to compare the blood pressure responses to two modes of

dynamic exercise in older lower fit vs. higher fit men and women. It was hypothesized that 1)

systolic blood pressures would increase more during small muscle mass exercise than large

muscle and 2) aerobic fitness would influence the blood pressure response in older adults in a

mode or sex-specific manner. Older (60-80 yrs) normotensive healthy men (higher fit n=12,

lower fit n=6) and women (higher fit n=13, lower fit n=12) were recruited. All subjects

performed treadmill and single-leg knee extensor exercise to fatigue on separate days. Systolic

and diastolic blood pressure were monitored during exercise and mean arterial blood pressure

was calculated by equation. The rise in blood pressure with exercise was quantified by slope

analysis using blood pressures during Stage 1 through 4 for each exercise mode. To normalize

the pressor response to exercise intensity the absolute pressures were normalized to METs

(multiples of resting oxygen uptake). Results indicated that all groups exhibited higher arterial

pressure responses during knee extensor exercise as compared to treadmill exercise. Fitness level

did not influence these responses during treadmill exercise, but did attenuate the rise in systolic

blood pressure during knee extensor exercise in older men, but not older women. In summary

these findings suggest that small muscle dynamic exercise elicits a higher blood pressure

response as compared to large muscle and fitness influences the response to small muscle mass

exercise in men but not in women.

Keywords: sex differences, pressor response

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INTRODUCTION

Dynamic exercise is accompanied by increases in arterial blood pressure that are

mediated by increased central command as well as feedback from active skeletal muscles (i.e.,

group III and IV afferents that are sensitive to mechanical and metabolic changes, respectively).

Arterial blood pressure during exercise is modulated by arterial baroreflexes that adjusts

sympathetic nerve activity within active and inactive skeletal muscle (1). The rise in blood

pressure with exercise serves to increase or maintain blood flow, but the pressor response can be

exaggerated in conditions associated with endothelial dysfunction (2-4).

Blood pressure responses to dynamic exercise are influenced by the size of active muscle

(5-6) such that the magnitude of the pressor reflex is inversely related to the size of active muscle

(7). Therefore, with respect to dynamic exercise, the blood pressure response to the use of a

large muscle mass has been shown to be less pronounced when compared to small muscle

activity (8-11). It is well known that this higher response with respect to the small muscle mass

exercise is far greater than the metabolic cost of the exercise. The observable difference exists

largely because of the whole body cardiovascular adjustments to the exercise stress (12). Large

muscle dynamic exercise elicits a large rise in heart rate and cardiac output accompanied by a

marked decline in total resistance (TPR). The reduction in TPR as a result of the systemic

vasodilatation to the large working muscle mass is the primary cause for the whole body decline

in blood pressure. During an exercise which involves the contraction and relaxation of only a

small muscle mass, there are only modest increases in heart rate and cardiac output accompanied

by little or no change in TPR. Because a large vasodilatory response is not stimulated, TPR does

not markedly decrease, and the blood pressure response does not fall dramatically.

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It is well known that age is associated with a rise in resting and exercise blood pressure.

With respect to resting blood pressure there is, on average, a 20 mm Hg systolic and 10 mm Hg

diastolic increment increase in blood pressure from age 30 to 65 years (13). In a cross-sectional

study of 10,355 people the average systolic pressure in those aged >65 years was 140 mmHg for

men and 150 mmHg for women; the average diastolic pressure was 70 mmHg in men and 80

mmHg in women (14). With regard to exercise much research has shown that there is a

heightened blood pressure response (especially systolic blood pressure) to graded dynamic

exercise in older men and women when compared to younger men and women (15). In addition,

it has also been found that this heightened BP response is more pronounced in older women (16).

It is well-known that training provides blood pressure lowering benefits with both normotensive

and hypertensive individuals (17-19) as well as for older individuals (20) during rest and exercise.

The purpose of the current investigation was to explore the systolic, diastolic, and mean

arterial blood pressure responses - defined by the slope values: absolute blood pressure across

working METs - to two modes of dynamic exercise in older men and women of different fitness

levels. Firstly, we wanted to conduct a focused observation on how the pressor responses

compared between two modes of dynamic work and ask whether the response was determined by

the active muscle, i.e. whether it might be more pronounced during knee extensor exercise

compared to treadmill in the aged. Secondly, we wanted to know if the heightened exercise

blood pressure response normally seen in older individuals was fitness dependent, i.e. to

determine if an increase in fitness level modulates the heightened blood pressure response seen

in older men and women, and if this fitness effect is mode or sex-specific.

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METHODS

Participants

Six lower fit older men (71 ± 2 yr), 12 higher fit older men (71 ± 2 yr), 12 lower fit older

women (67±1 yr), and 13 higher fit older women (67±1 yr) were recruited for this study. All

participants were normotensive (< 140/90 mmHg), and were apparently healthy as evaluated by

medical history questionnaire, a physical examination, and resting electrocardiogram. All

participants provided written consent to participate in the study after receiving an explanation of

the experimental procedures and possible risks associated with participation. This study was

approved by the Office for Research Protections at Pennsylvania State University in agreement

with the guidelines set forth by the Declaration of Helsinki.

Treadmill Exercise Testing

Each participant performed a modified Balke treadmill test to peak effort. This graded

test consisted of a 4 minute warm-up at 2.5 mph followed by adjustment of the speed to elicit

~75% of age-predicted peak heart rate after which the intensity of exercise increased every 2

minutes (2% increase in elevation) until the participants reached volitional fatigue.

Blood pressures were measured via auscultation during the second minute of each

exercise stage. Blood pressure measurements were not attempted during peak effort to enable

participants to fully engage both arms and give maximum effort without disturbance. Pulmonary

oxygen uptake (VO2) was measured using analysis of expired gases by a Parvomedics metabolic

cart (Sandy, Utah).

Knee Extensor Exercise

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Each participant performed single leg knee extensor exercise as described previously (21-

22). To begin, participants were seated in a semi-reclined position with knees flexed at an angle

of 90. To avoid extraneous movement during the exercise participant’s torso and thighs were

strapped to the chairs. Knee extensions through a nearly full range of motion (90–170) were

performed at 40 contractions per minute with the left foot placed in a boot that was connected to

the pedal arm of a cycle ergometer (Monark) that was placed behind the subject. The exercise

protocol consisted of three minute stages. The first stage consisted of quiet rest, followed by

unloaded passive exercise (manual external movement of lower leg), knee extensions against no

resistance (0 W), and finally extensions as resistance increased incrementally until the subject

could no longer maintain cadence. After each three minute stage work rate increased by 10 W for

men and 5 W for women.

Blood pressures were measured continuously at rest and during exercise using radial

tonometry of the right hand by a Finometer MIDI (Finapress Medical Systems, Netherlands).

The blood pressure waveform at rest was calibrated against multiple measurements taken by an

IntelliSense blood pressure monitor (Omrom, Vernon Hills, Illinois). Beat by beat blood pressure

was collected on-line at a sampling frequency of 400 Hz and stored using a Powerlab system

(ADInstruments, Castle Hill, Australia).

Data Analysis and Computations

All blood pressure calculations were derived from average values taken over the last 30

seconds of rest, passive exercise, and each work rate. Slope values were calculated using blood

pressure values taken during exercise (treadmill: between stages 1 and 4; knee kick: first 4

stages). Those participants who did not complete as least three stages were not included in the

slope analysis.

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Statistical Analysis

Significance was accepted at P < 0.05 for all statistical analyses. Microsoft Excel was

used to perform all analyses. A one-tailed paired t-test was used to test for mode-specific

differences. A two-sample independent t-test was used to test for significant between group

differences.

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RESULTS

Descriptive Characteristics (Table 1)

Anthropometric characteristics of the participants are presented in Table 1. Higher and

low fit men were similar age, but lower fit women were older than higher fit women (P <0.05).

Both higher and low fit groups were of similar weight and height, however, the lower fit group

had a higher percent body fat than the higher fit within each sex (P <0.05).

Peak Exercise Responses (Table 2)

Table 2 displays group average data for peak exercise responses divided by mode of

exercise. As a result of study design the lower fit group had a lower peak aerobic capacity (peak

VO2) during treadmill exercise than the higher fit group within each sex (P <0.05). Similarly, the

peak VO2 (ml/kg/min) and work rate achieved during knee extensor exercise was lower in the

lower fit group as compared to the higher fit group within each sex (P <0.05). The difference in

peak VO2 during knee extensor exercise showed sex-specific differences based on the

expression of VO2.

Influence of the active muscle mass on the pressor response

Relationships between the arterial blood pressure responses to both modes of dynamic

exercise are displayed in Figure 1. Blood pressure increased during both small muscle and large

muscle exercises in all groups. This pressor response was significantly (P <0.05) more

pronounced during knee extension exercise as compared to treadmill exercise in older men

(Figure 1A) and older women (Figure 1B) independent of fitness level.

Influence of fitness and sex on pressor response in older adults

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Fitness did not influence the blood pressure response to treadmill exercise. Thus, a higher

BP response was not observed in low fit older adults vs. high fit older adults irrespective of sex.

During knee extension exercise fitness influenced the pressor response in older adults in a

sex-specific manner such that lower fit older men had a higher blood pressure response than

higher fit men (P <0.05). This observation was not found for women (P = 0.17).

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DISCUSSION

In the present investigation we examined the arterial blood pressure responses to graded

dynamic exercise in older (60-79 yr) normotensive groups of women and men. Consistent with

prior research involving healthy younger individuals, we observed greater intensity-dependent

increases in systolic and mean pressures during small muscle mass dynamic exercise (single leg,

knee extensor exercise) compared to whole body dynamic exercise (standardized treadmill

testing). Aerobic fitness attenuated the rise in systolic and mean pressures during small muscle

mass exercise in older men, but had no apparent influence on these responses during large

muscle mass exercise in either sex. Moreover, aerobic fitness level had no measurable influence

on pressor responses to either large or small muscle mass exercise in older women. Collectively,

these are novel findings which have implications for understanding the determinants of, and

potential countermeasures for, sex-specific age differences in blood pressure reactivity to

exercise.

Pressor responses to dynamic exercise: Influence of active muscle size

All subjects exhibited larger exercise pressor responses, defined as the total rise in SBP

and MAP per MET through 3 (women) or 4 (men) stages, during knee extensor exercise than

those observed during treadmill exercise. This finding is not surprising given that 1) arterial

pressure during dynamic exercise is thought to be regulated primarily as a function of relative

work intensity (Bezucha et al 1982; Lewis et al 1983, 1985; etc) and 2) that a one-MET increase

during knee extensor exercise represents a much larger % of an individual’s working range

during that mode of exercise (peak METS = ___ to ___) compared to treadmill exercise (peak

METS = __ to __). However, even when mode differences in peak metabolic capacity in the

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present study were accounted for (SBP or MAP vs. % of mode-specific VO2peak or peak METS),

the mode differences in exercise blood pressures persisted in all four groups IS THIS TRUE?

We will also want to know if the slopes of the SBP and MAP responses vs. % of VO2peak

differ between modes (overall and within groups)….the reason for this will become clearer

below).

No prior studies have directly compared cardiovascular responses to graded knee

extensor and treadmill exercise to allow comparisons with the present findings. However, the

greater blood pressure responses observed during single knee extensor exercise in the present

study (across all groups) are likely reflective of a greater use of accessory (stabilizing) muscles;

such an influence could elevate arterial pressure by central (greater volitional effort, HR) and/or

peripheral (vascular compression and metaboreflex stimulation) mechanisms. Further insight

into the former possibility will be explored by comparing the HR response (rise in HR per unit

increase in VO2 or MET) to knee extensor exercise in relation to the HR response to treadmill

testing. If the overall HR response to knee extensor exercise is exaggerated (and if the RPE vs. %

of peak workload relationship is steeper during knee extensor vs. treadmill exercise; Stebbins et

al AJP 2002), this would support the interpretation that greater pressor responses during knee

extensor exercise are due, at least in part, to greater recruitment and/or isometric involvement of

stabilizing muscles.

Pressor responses to large muscle dynamic exercise: influence of fitness

Systolic, diastolic and mean arterial blood pressures of aerobically trained young adults

are generally lower at any given submaximal (same absolute) workload or VO2 compared to their

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sedentary peers; this reflects a reduction in total systemic vascular resistance since cardiac output

at a given submaximal workload does not change with aerobic training (refs). Exaggerated

pressor responses at submaximal exercise loads have been observed in adults with a higher

proportion of fast-twitch, low oxidative fibers in their leg musculature (ref) and in younger adults

at risk for future hypertension (i.e., familial hypertension) who also have low calf muscle

vasodilatory capacities (Bassett et al), suggesting a possible link between exercise blood pressure

and the structural and/or functional capacity of the leg muscles to vasodilate in young (currently

normotensive) adults. It is important to note that most of the literature examining these

relationships in younger adults has been conducted in men; relatively little is known about the

determinants of exercise blood pressure in younger women (confirm that this statement is true,

Martin et al included younger fit and sedentary women).

Several studies have reported lower blood pressure responses at fixed submaximal

workloads in aerobically trained compared to sedentary, but normotensive older men (Hagberg et

al 1985; Ogawa et al 1992; Martin et al 1991). Martin et al (ref) for example, observed 15-18%

lower systolic, and 10 to 14% lower mean blood pressures at the same submaximal treadmill

stages in aerobically trained vs. untrained older men (a smaller, but significant fitness effect was

observed in their younger men as well). In the current study, we did not observe a significant

fitness difference in blood pressure responses to treadmill exercise in older men, when expressed

as a unit change in blood pressure per MET (figure) (is this true when we look at BP responses

vs. treadmill VO2?). The lack of a significant fitness effect on submaximal blood pressure

responses to treadmill testing in the present groups of older men is difficult to explain, but could

reflect a) the relatively low sample size of our low-fit older group, b), the lack of a significant

age group difference in the first place (data for younger groups not shown) and/or c) the higher

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resting systolic and mean arterial pressures of the higher fit older group (vs. all other groups;

Table 1; we may need to control for resting BP differences via ANCOVA).

Blood pressures at similar relative work intensities were not significantly influenced by

fitness in older men (figure), consistent with most of the literature for both weight bearing

(Ogawa et al 92; Martin et al 1991, etc) and non-weight bearing (Hagberg et al 1985?, Proctor et

al Mayo study) exercise. However, it is interesting to note that the rise in MAP at 80% of

treadmill VO2max (i.e., delta increase from rest) appeared to be markedly less (insert p-value) in

our higher men than it was in our lower fit older men. Collectively, this comparison reflects the

importance of taking resting (baseline) blood pressure and relative exercise intensity into account

when interpreting the pressor responses to exercise in older adults.

There was no fitness effect on treadmill exercise blood pressure responses in older

women, regardless of how the data were examined or analyzed. The lack of an aerobic fitness

effect on blood pressures of older women during submaximal exercise is consistent with results

of Ogawa et al (ref). In their study, systolic, diastolic and mean pressures during Bruce treadmill

stages 1 and 2 were no different in older fit vs. sedentary women, despite the markedly elevated

responses of these groups compared to younger controls (ref). Our older female groups were

relatively similar in age, body size and composition, and cardiorespiratory fitness (treadmill

VO2max per kg FFM; will need to check each of these statements) to the subjects studied by

Ogawa et al (ref) and similar mean arterial pressures at comparable work intensities (is this

statement true?....compare their data at Bruce protocol stage 1 and 2 vs. our data at similar

MET levels). However, these findings appear to be at odds with the results of a large cross-

sectional study of women (Kokkinos et al 2002) in which fitness level (age-adjusted treadmill

time to exhaustion) was a significant determinant of systolic blood pressure at a fixed

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submaximal workload (Bruce protocol stage 2 = 6-7 METS). Reasons for such disparate

findings are unclear, but the inclusion of an extremely wide age range of participants in the

Kokkinos et al study (20 to 80 yr) could obscure the influence of fitness on pressor responses in

older women per se. Aerobic exercise training programs sufficient to significantly increase

systemic aerobic capacity (treadmill VO2max) generally do result in improved hemodynamic

responses (i.e., reduced arterial pressures and rate pressure product) to exercise in younger and

middle-aged women (find refs), but the findings in studies of exclusively older, post-menopausal

women have been less consistent and often show attenuated cardiac (Spina et al papers) and local

vascular (Martin et al 1991) adaptations to conventional aerobic exercise training interventions.

Martin et al suggested that the remediative effects of aerobic training on vascular function might

depend on the presence of estrogen since a sub-sample of their subjects who had taken estrogen

therapy exhibited slightly lower exercise blood pressures and higher muscle dilator capacities

than the estrogen deficient women did. Thus, the lack of any apparent fitness modulation on

hemodynamic responses during large muscle mass exercise in the older estrogen deficient

women we studied was not entirely unexpected.

Pressor responses to small muscle dynamic exercise: influence of fitness

The literature on aging and blood pressure responses to small muscle mass exercise are

limited primarily to isometric contractions of the forearm musculature in men (Taylor et al 1991;

Petrofsky & Lind 1975). In those studies, the magnitude of rise in arterial pressure during

sustained contractions at 40% of maximum voluntary handgrip force was very similar in healthy

younger compared to older men matched for peak forearm strength. Differences in active

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muscle groups (arm vs. leg), type of contraction (static vs. dynamic), and aging-related muscle

function (preserved vs. reduced) between the present study and that of Taylor et al (ref) make it

very difficult to compare findings. Nonetheless, it was interesting to find evidence in the present

study for a fitness effect in the older men, but not in their female peers during dynamic knee

extensor exercise. Why fitness would exert a greater influence on the pressor responses to

graded knee extensor vs. treadmill exercise in older men is not immediately obvious, nor is the

lack of such an influence in older women. However, the relatively large systolic and especially

diastolic pressure responses to isolated quadriceps exercise in older low-fit women (figure 1)

suggests a greater hemodynamic load on their heart (compared to higher fit women and men)

during activities that specifically stress this functionally important muscle group (Kokkinos et al

ref, etc; we should also examine rate pressure product as an index of myocardial O2

demand).

ACKNOWLEDGEMENTS

The authors would like to thank the participants,

GRANTS

This research was supported by National Institute on Aging Grant (NIA) R01 AG-

0182446 (to D.N. Proctor, and Division of Research Resources Grant M01 RR-10732 (to GCRC).

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Table 1. Participant characteristics

Men Women

Higher Fit

(n=12)

Lower Fit

(n=7)

Higher Fit

(n=13)

Lower Fit

(n=12)

Age (yr) 63.8 ± 1.1 66.3 ± 2.3 63 ± 1 68.3 ± 1.8*

Weight (kg) 79.8 ± 3.3 82.1 ± 4.3 63.3 ± 1.6 64 ± 2.8

Height (cm) 178 ± 1.9 175 ± 1.9 161.3 ± 2.1 160.9 ± 1.4

Body fat (%) 20.5 ± 1.1 25.6 ± 1.2* 32.4 ± 0.8 37 ± 1.5*

Fat free mass (kg) 61.4 ± 1.9 59.5 ± 2.6 44.2 ± 2.1 39.3 ± 1.3

Quadriceps mass (kg) 2.5 ± 0.1 2.4 ± 0.2 1.8 ± 0.1 1.8 ± 0.1

Blood Pressure (mmHg)

Resting Systolic 134.8 ± 2.7 122.4 ± 2.8* 129.1 ± 4.1 129.2 ± 4.6

Resting Diastolic 80.8 ± 1.4 76.9 ± 2.0 72.3 ± 1.8 73.2 ± 3.6

Resting Mean Arterial 98.8 ± 1.8 91.9 ± 2.4* 91.2 ± 8.9 91.8 ± 3.3

Values are mean ± SEM. *, significant difference between high and lower fit older adults within each sex

(P < 0.05).

Table 2. Peak exercise responses

Men Women

Higher Fit

(n=12)

Lower Fit

(n=7)

Higher Fit

(n=13)

Lower Fit

(n=12)

Treadmill

VO2 (L/min) 3.2 ± 0.1 2.3 ± 1.3* 2.0 ± 0.1 1.5 ± 0.1*

VO2 (ml/kg/min) 40.2 ± 1.4 28.2 ± 1.5* 31.2 ± 0.8 23.2 ± 0.7*

VO2 (ml/min/kg FFM) 52 ± 1.8 39 ± 2.3* 45.6 ± 2.2 37.5 ± 1.1*

Knee Kick

Final work rate (Watts) 46.7 ± 2.2 36.7 ± 4.2* 30 ± 1.5 24.2 ± 1.7*

VO2 (L/min) 0.92 ± 0.03 0.75 ± 0.03* 0.61 ± 0.03 0.55 ± 0.04

VO2 (ml/kg/min) 11.6 ± 0.5 9.1 ± 0.3* 9.7 ± 0.3 8.7 ± 0.4*

VO2 (ml/min/kg QMM) 36.8 ± 1.8 31.9 ± 2.2* 35.4 ± 2.1 31.9 ± 1.8

Values are mean ± SEM. VO2: oxygen uptake; FFM: fat free mass; QMM: quadriceps muscle mass. *,

significant difference between high and lower fit older adults within each sex (P ≤ 0.05).

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FIGURE LEGENDS

Figure 1 The rise in blood pressure (systolic blood pressure, SBP) across METs during treadmill

and knee extensor exercise. (A) The pressor response was higher during knee extensor as

compared to treadmill exercise. There was no difference in the rise of blood pressure between

low fit (n=6) and higher fit (n=12) men during treadmill exercise, but lower fit old men had a

higher blood pressure response to knee extensor exercise than high fit men. (B) The pressor

response was higher during knee extensor as compared to treadmill exercise. There was no

difference in the rise of blood pressure between low fit (n=12) and high fit (n=13) women during

treadmill and knee extensor exercise. *, significant difference between treadmill and knee

extensor exercise (P < 0.05). †, significant difference between low and high fit older men (P <

0.05).

M en

A ge G roup

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*

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