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Am J Physiol Heart Circ Physiol 287: H735-H740, 2004. First published March 11, 2004; doi:10.1152/ajpheart.00959.2003
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Effect of aging on renal blood flow velocity during static exercise

Afsana Momen,1 Urs A. Leuenberger,1 Brian Handly,1 and Lawrence I. Sinoway1,2

1Division of Cardiology, Pennsylvania State University College of Medicine, Milton S. Hershey Medical Center, Hershey 17033; and 2Lebanon Department of Veterans Affairs Medical Center, Lebanon, Pennsylvania 17042

Submitted 9 October 2003 ; accepted in final form 6 March 2004


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
During exercise, activation of the sympathetic nervous system causes reflex renal vasoconstriction. The effects of aging on this reflex are poorly understood. This study evaluated the effects of age on renal vasoconstrictor responses to handgrip. Seven older (65 ± 9 yr) and nine younger (25 ± 2 yr) subjects were studied. Beat-by-beat analyses of changes in renal blood flow velocity (RBV; duplex ultrasound) were performed during two handgrip paradigms. Arterial blood pressure (BP) and heart rate were also measured, and an index of renal vascular resistance (RVR) was calculated (BP/RBV). In protocol 1, fatiguing handgrip [40% of maximal voluntary contraction (MVC)] caused a greater increase in RVR in the older subjects (old 90% ± 15 increase, young 52% ± 4 increase; P = 0.03). During posthandgrip circulatory arrest (isolates muscle metaboreflex), the increases in RVR were only ~1/2 of the increase seen at end grip. In protocol 2, 15-s bouts of handgrip at graded intensities led to increases in RVR in both subject groups. This effect was not seen until 50% MVC workload (P < 0.05). RVR responses occurred early and were greater in older than in younger subjects at 50% MVC (32 ± 6% vs. 16 ± 5%; P = 0.02) and 70% MVC (39 ± 11% vs. 24 ± 8%; P = 0.02). Static exercise-induced renal vasoconstriction is enhanced with aging. Because the characteristics of this response suggest a predominant role for mechanoreceptor engagement, we hypothesize that mechanoreceptor responses are augmented with aging.

kidney; sympathetic nervous system

DURING EXERCISE, the sympathetic nervous system is activated. Two neural mechanisms are involved in this process. A feed-forward system termed central command activates the sympathetic nervous system in parallel with activation of {alpha}-motoneurons (31). The other mechanism, the exercise pressor reflex, evokes sympathetic activation in response to reflex engagement of mechanically and metabolically sensitive muscle nerve afferents within active skeletal muscle (2, 13, 15).

As in younger subjects, exercise evokes sympathoexcitation in older subjects. However, in older subjects the increases in muscle sympathetic nerve activity (MSNA) with exercise have been reported to be similar (23, 27) or less (20, 26) compared with younger subjects. A prior report from this laboratory (20) showed attenuated sympathetic nerve responses in the aged. It was suggested that this was due to reduced engagement of the muscle metaboreflex.

During static exercise, reflex renal vasoconstriction takes place to maintain blood pressure (BP) as well as redistribute blood flow to metabolically active skeletal muscle beds. Recent studies in healthy young volunteers (22) demonstrate that renal vasoconstriction during exercise is due primarily to sympathetic vasoconstriction, which in turn is due to engagement of mechanosensitive muscle afferents within the contracting muscle. In the present study, we examined renal hemodynamics during static exercise in older and younger subjects to determine whether the reflex renal vasoconstriction during handgrip is influenced by the aging process. The renal vascular response to static exercise was considered as a surrogate marker for efferent sympathetic outflow to the kidney because direct recordings of renal sympathetic nerve activity cannot be performed in humans. The results of the present study suggest that renal vasoconstrictor responses are exaggerated in the elderly, an effect we believe is due to heightened engagement of the muscle mechanoreflex.


   METHODS
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 METHODS
RESULTS
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Study Population

Nine young (5 men, 4 women; age 25 ± 1 yr, mean body mass index 23 ± 1 kg/m2) and seven older (4 men, 3 women; age 65 ± 3 years, body mass index 23 ± 1 kg/m2) subjects were studied. All were normotensive nonsmokers and were on no medication. All were involved in routine physical activity. None of the subjects had diabetes or cardiovascular or renal disease. Each subject provided informed written consent to participate in the study, which was approved by the Milton S. Hershey Medical Center's institutional review board.

Renal Blood Flow Velocity

Duplex ultrasound (HDI 5000; ATL Ultrasound, Bothell, WA) was used to obtain beat-by-beat recordings of changes in mean renal blood flow velocity (RBV; cm/s) in each subject as described previously (22). The renal artery was scanned by the anterior abdominal approach. A curved array C5-2 MHz Doppler probe with a 2.5-MHz pulsed Doppler frequency was used. The probe insonation angle to the renal artery was kept at ≤60. To obtain the highest-quality Doppler tracings possible, the transducer was maintained in a constant position. Within each subject, the data were obtained in the same phase of the respiratory cycle. Software developed for the HDI 5000 was used to analyze Doppler signals. Renal vascular resistance (RVR) was calculated as the quotient of mean arterial pressure (MAP) and the respective mean RBV. RVR was expressed in arbitrary units (AU). Continuous recordings of heart rate (HR; electrocardiogram) and BP (Finapres; Ohmeda, Madison, WI) were obtained throughout all protocols. Resting BP was measured with an automated sphygmomanometer (Dinamap; Critikon, Tampa, FL). A force transducer was used to determine the force of muscle contraction.

Study Protocols

Protocol 1: Fatiguing static handgrip exercise followed by posthandgrip circulatory arrest. After a 5-min collection of baseline HR, MAP, and RBV, subjects started static handgrip exercise (nondominant forearm) at 40% of maximum voluntary contraction (MVC) and continued gripping until they were unable to maintain the given tension. At the end of contraction, all subjects graded their perceived level of exertion as 20 (maximal effort) on the Borg scale (6). Immediately before the gripping exercise ended, posthandgrip circulatory arrest (PHG-CA) was initiated by inflating a previously placed arm cuff to ~250 mmHg. The cuff was kept inflated for 2 min.

Protocol 2: static handgrip exercise at graded intensities. After baseline data were collected, subjects performed single 15-s bouts of static handgrip exercise at 10%, 30%, 50%, and 70% of the respective subject's MVC. The same sequence was maintained in all subjects. The interval between each handgrip bout was ~1 min.

Protocols 1 and 2 were performed on the same day. The time difference between the two protocols was ~15 min.

Data Analysis and Statistics

Beat-by-beat sequential analyses of HR, MAP, RBV, and RVR were performed for all subjects. Baseline values for each parameter were the average data values obtained during the 5-min rest period before the beginning of each exercise paradigm.

In the fatiguing static handgrip protocol, HR, MAP, RBV, and RVR were analyzed as previously described (22). Briefly, each variable was measured around the time that represented 10%, 20%, 40%, 60%, 80%, and 100% (peak) of the respective subject's time to exhaustion. Data from the last 15-s time period during circulatory arrest were used in the statistical analysis.

Data are presented as means ± SE. Resting values between young and older subjects were compared by unpaired t-tests. Repeated-measures one-way ANOVA and Dunnett's test were applied to compare variables to baseline in individual groups. Repeated-measures two-way ANOVAs were applied for each variable to test for two main effects: age (between older and younger subjects) and the stage of the respective handgrip paradigm. To compare older and younger subjects, tests of simple effects were performed at the respective time periods of the gripping paradigms. The level of significance was set at P < 0.05.

In the protocol with handgrip at graded intensities, data were analyzed in 5-s time periods. Statistical analyses were performed separately on each 5-s period (i.e., 0–5, 6–10, and 11–15 s).


   RESULTS
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DISCUSSION
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Baseline characteristics are presented in Table 1. Resting values of MAP, HR, RBV, RVR and MVC did not differ significantly between younger and older subjects.


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  		Table 1. Resting data in younger and older subjects

 
Protocol 1: Static Fatiguing Handgrip Followed by PHG-CA

The time to fatigue at 40% MVC was 97 ± 6 and 115 ± 16 s [P = not significant (NS)] for younger and older subjects, respectively. During fatiguing handgrip (40% MVC), increases in RVR were noted for both younger and older subjects (paradigm effect, P < 0.002; Fig. 1A). A one-way ANOVA analysis followed by Dunnett's test in the two subject groups demonstrated a significant increase in RVR in the older group at 10% time to fatigue (1.81 ± 0.14 vs. 2.22 ± 0.24; P = 0.014). Although not statistically significant, the RVR response also tended to be higher (1.84 ± 0.20 vs. 2.09 ± 0.24; P = NS) in the younger group. Despite the fact that the RVR response at 10% time was not significantly different from baseline in the younger group, each individual 10% RVR was higher than the respective control value. A two-way ANOVA demonstrated an age main effect during fatiguing handgrip (Fig. 1A). Post hoc analyses demonstrated that at the 80% and 100% time points RVR was greater in the older subjects than in the younger subjects. Similarly, the reduction in RBV was also greater in the older subjects (age main effect: P < 0.022; Table 2). Although MAP and HR increased during handgrip in both groups, no effect of age was seen for these parameters (Table 2).



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  		Fig. 1. A: %change in renal vascular resistance index (y-axis) as a function of %time to fatigue (x-axis) during static handgrip [40% maximal voluntary contraction (MVC)]. Data are presented as means ± SE. P value for 2-way ANOVA: *significant difference between older (n = 7) and younger subjects (n = 9). ns, Not significant. B: comparison of baseline and posthandgrip circulatory arrest (PHG-CA) vascular resistance. *P < 0.05.

 

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  		Table 2. Protocol 1 of fatiguing static handgrip HR, MAP, and RBV data

 
Although a significant paradigm effect was noted for RVR value, no effect of age was noted during PHG-CA (Fig. 1B). In both groups, RVR values during PHG-CA represented only one-half of the RVR response seen at end grip. Increases in RVR at end grip and at 2 min of PHG-CA from baseline were 90 ± 15% (baseline vs. end grip: 1.81 ± 14 vs. 3.52 ± 55 AU) and 48 ± 17% (baseline vs. PHG-CA: 1.81 ± 14 vs. 2.76 ± 55 AU) in the older group and 52 ± 4% (baseline vs. end grip: 1.84 ± 20 vs. 2.77 ± 25 AU) and 28 ± 6% (base vs. PHG-CA: 1.84 ± 20 vs. 2.39 ± 34 AU) in the younger group, respectively. Other variables during PHG-CA are shown in Table 3.


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  		Table 3. Minute 2 of PHG-CA during protocol 1

 
Protocol 2: Static Handgrip Exercise at Graded Intensities

Significant increases in vascular resistance were found in both younger and older subjects after 5 s of onset of short bouts of handgrip (15 s) exercise at 50% and 70% of MVC (Table 4). There was a strong tendency toward an increase in RVR in the older subjects during the first 5 s (1-way ANOVA main effect; P = 0.051).


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  		Table 4. Raw data from protocol 2: static handgrip (15 s) at graded intensities

 
Older subjects had greater increases in vascular resistance (Fig. 2) and greater reductions in RBV (Table 5) than younger subjects (age main effect: P < 0.05). No effect of age was seen on the data for HR or MAP, except that the increase in HR was found to be less in older than younger subjects during the first 5 s at 70% MVC (Table 5).



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  		Fig. 2. Percent change in renal vascular resistance index (y-axis) due to 15-s bouts of static handgrip at 10%, 30%, 50%, and 70% MVC (x-axis) in older and younger subjects. Data were examined separately for 0–5 (A), 6–10 (B), and 11–15 (C) s. Main effects and interactions are shown.

 

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  		Table 5. Percent change data from protocol 2: static handgrip (15 s) at graded intensities

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 REFERENCES
 
The important new finding in this study is that RVR increased more with exercise in the older subjects than in the younger subjects (Figs. 1A and 2). The differences were more pronounced during handgrip at higher intensities as well as near the end of fatiguing handgrip. The RVR responses were seen early, and PHG-CA-induced muscle metaboreflex engagement did not evoke a major rise in vasoconstriction in either group. Thus the findings of this study confirm previous work suggesting that muscle mechanoreflex activation is the predominant mechanism responsible for renal vasoconstrictor response during handgrip exercise (22).

Protocol 1: Static Fatiguing Exercise Followed by PHG-CA

No difference in baseline RVR was noted in older and younger subjects. This is consistent with prior work done by Esler et al. (9a). These authors found similar renal norepinephrine outflow in young and aged humans. However, our resting RVR findings are at odds with those of other human studies (1, 5, 8, 10, 14). These previous studies showed higher resting RVR in the older group compared with the younger group. The exact reason for these incongruences is not clear, although methodological issues must be considered.

In our study, we used RBV as our index of renal blood flow. Because of limited spatial resolution of the Doppler system used, we could not measure renal artery diameter and thus we could not measure renal blood flow directly. Therefore, we cannot exclude the possibility that renal artery diameter decreases with age. If this were the case, then even though flow velocity was similar in the two groups, total flow could have been lower in the aged. However, our primary goal was to determine the changes in renal vasoconstrictor responses during different muscle contraction paradigms. Because conduit vessel diameter does not change during renal maneuvers that evoke a rise in RVR (21), we believe that changes in RBV reported for the two study groups are reflective of changes in renal blood flow during static exercise.

During fatiguing exercise, RVR increased in both young and older subjects. The increase in RVR was significantly greater in the older subjects at the 80% and 100% time periods, yet the RVR values during PHG-CA were similar in the two groups. This makes it unlikely that the age effect is due to enhanced engagement of the metaboreflex with aging. Because we found an increase in RVR early in exercise (<15 s at 10% time to fatigue), we presume that central command and/or muscle mechanoreflex mechanism played the crucial role to evoke enhanced vasoconstriction in the aged subjects. A prior study suggests that increases in HR during initial phases of handgrip exercise are reflective of increases in central command (19). Because HR responses were not greater (during protocol 1) in the aged, we would conclude that the greater RVR responses seen in the aged were not due to central command but rather to mechanoreflex activation. Specifically, we postulate that at the end of exercise, the greater increase in RVR in the older subjects was due to a greater level of efferent response for a given level of mechanical deformation of the afferent receptive field when the deformation occurs in the presence of metabolic by-products of muscle contraction (3). Prior animal studies have also shown that mechanosensitive muscle nerve afferents are sensitized by metabolic products during static contraction, e.g., ATP (18), lactic acid (24, 28), and arachidonic acid (25).

Graded Intensity of Static Handgrip Exercise

The findings in the present study in both groups replicate our previous findings that renal vasoconstriction was seen early in muscle contraction and had an MVC threshold (Table 4; Ref. 22). Using isolated perfused kidneys of younger and older rats, Eikenberg (9) observed similar renal vascular responses for a given degree of renal sympathetic nerve stimulation despite increased norepinephrine overflow in older rats. The findings in this prior report suggest that renal vascular adjustments are dependent on changes in renal sympathetic nerve activity (9).

We speculate that the larger RVR responses seen in the older subjects during the short bouts of handgrip were due to an engagement of a neural system with a short onset latency such as central command or the muscle mechanoreflex. It should be noted that larger RVR responses with handgrip in the older subjects were not associated with a greater increase in HR. However, during the initial 5 s of handgrip at 70% MVC (Table 5), increases in HR were significantly smaller in the older subjects compared with the younger subjects. Therefore, it is unlikely that a greater central command response was responsible for eliciting the augmented renal vasoconstrictor responses observed in the older subjects. Furthermore, in a previous study using involuntary biceps contraction protocol, we (22) demonstrated that central command is not necessary to evoke renal vasoconstriction during early muscle contraction. Thus we postulate that the enhanced renal vasoconstriction in the older subjects during short bouts of exercise was primarily due to engagement of the muscle mechanoreflex.

In a recent report from this laboratory (20), we demonstrated that muscle metaboreflex regulation of MSNA is attenuated in the aged. The reasons why the mechanoreflex is augmented and the metaboreflex is attenuated are not clear. Important questions raised by these findings are as follows. 1) Is the mechanism responsible for the attenuated metaboreflex response in the aged linked to the augmented mechanoreflex response? 2) Are these findings linked to differences in muscle fiber type seen with aging? 3) Are these responses in the aged due to differences in receptor population in this group?

It is interesting to note that skeletal muscle becomes more oxidative with aging (4, 12, 30). Moreover, it has been demonstrated that oxidative muscle has a higher collagen content then nonoxidative muscle (32) and that with aging the collagen content of oxidative muscle is greater than that of nonoxidative muscle (17). Moreover, type I collagen (would allow greater mechanical deformation within the receptive field of a given muscle afferent) was found to have a greater contribution to the age-related accumulation of total muscle collagen (16). We speculate that the greater collagen content in the extracellular matrix may increase this deformability of the group III afferents whose receptor fields reside within the interstitium of the aged phenotypically oxidative muscle.

It has also been demonstrated that aging is associated with upregulation of the P2X3 purinergic receptor subtype in the rat prostate (29). It is this subtype that may be most important in mediating mechanoreceptor processes in sensory afferents (7, 11, 18). Thus it is possible that part of the increase in mechanoreceptor-mediated responses in the aged could be due to increased skeletal muscle P2X3 receptor expression.

We should also emphasize that in the present study we could not directly determine the effect of central command on renal vasoconstrictor responses in the older subjects. This was because, in many of the older subjects tested, electrical stimulation of the biceps muscle evoked small increases in muscle tension.

In conclusion, the novel finding in this report is that renal vasoconstrictor response to handgrip exercise is greater in older subjects compared with younger subjects. Because the vasoconstrictor response was seen early in static contraction protocols and PHG-CA response represents only one-half of the total vasoconstrictor response, our results are consistent with the concept that mechanically sensitive muscle afferents play an even more important role in evoking renal vasoconstriction in the elderly than they do in young subjects.


   GRANTS
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 ABSTRACT
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 RESULTS
 DISCUSSION
 GRANTS
REFERENCES
 
This work was supported by National Institutes of Health (NIH) Grants R01 AG-012227 (Sinoway), R01 HL-070222 (Sinoway), K24 HL-004011 (Sinoway), and NIH-National Center for Research Resources Grants M01 RR-010732 and C06 RR-016499.


   ACKNOWLEDGMENTS
 
The authors are grateful to Jennifer Stoner for expert manuscript preparation and to Kristen Gray and Michael Herr for technical support.


   FOOTNOTES
 

Address for reprint requests and other correspondence: L. I. Sinoway, Cardiology, H047, Penn State College of Medicine, PO Box 850, Hershey, PA 17033 (E-mail: lsinoway{at}psu.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.


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00959.2003v1
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