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The Effect of Water Immersion during Exercise on Cerebral Blood Flow

PUGH, CHRISTOPHER J. A.1; SPRUNG, VICTORIA S.1, 2; ONO, KUMIKO3; SPENCE, ANGELA L.1; THIJSSEN, DICK H. J.2, 4; CARTER, HOWARD H.1; GREEN, DANIEL J.1, 2

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Medicine & Science in Sports & Exercise: February 2015 - Volume 47 - Issue 2 - p 299-306
doi: 10.1249/MSS.0000000000000422
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Abstract

Exercise induces recurrent increases in blood flow and shear stress in micro- and macrovessels of the peripheral circulation. Episodic increases in endothelial shear stress represent a dominant stimulus for enhanced nitric oxide bioavailability, which is associated with improved cardiovascular health (18,19). Exercise has also been reported to have a beneficial effect on cerebral function (20,24), with some animal studies relating such benefits to enhanced cerebrovascular endothelial function (3,11,13,17,25).

During mild- to moderate-intensity exercise (<=60% maximal oxygen uptake), cerebral blood flow increases globally by approximately 10%–20% in response to increases in neuronal activation and cerebral metabolism (29,31,34). Although some studies indicate that regional differences might exist within the cerebral circulation during exercise (34,42,43), the prominent mechanisms driving the increase in global cerebral blood flow during exercise seem to be related to alterations in cerebral neuronal metabolism, partial pressure of arterial carbon dioxide, and/or arterial pressure (29,31,36).

Water-based exercise is a non–weight-bearing exercise modality for individuals with impaired functional capacity, which has emerged as a popular alternative for the management of clinically vulnerable groups (23). Previous studies have compared physiological responses to water- and land-based exercises in healthy (4–6,12,14,27) and diseased populations (7,10,16,35,40), but no previous study has reported the effect of water-based exercise on cerebral blood flow velocity (CBFv) using transcranial Doppler. This is of particular importance because we recently demonstrated that water immersion under resting conditions induces an increase in middle and posterior cerebral artery velocities (MCAv and PCAv, respectively), which is associated with elevated mean arterial pressure (MAP) and end-tidal carbon dioxide (8). The purpose of this study was therefore to examine the effect of an acute bout of land-based exercise versus exercise during water immersion on CBFv in healthy volunteers. We hypothesized that exercise performed during water immersion would be associated with augmented CBFv compared with land-based exercise.

METHODS

Participants

Fifteen healthy participants were recruited to the study (eight males; age, 26 ± 4 yr; body mass index, 24.3 ± 1.9 kg·m-2). All participants were normotensive, recreationally active (<=2 h·wk-1 of physical activity), nonsmokers with no history of cardiovascular, musculoskeletal, or metabolic disease or any contraindications to exercise. None of the participants reported taking any (prescribed) medication. Female participants were tested during the early follicular phase of the menstrual cycle, defined as days 1–7 of the menstrual cycle. The study conformed to the Declaration of Helsinki and was approved by the human research ethics committee of the University of Western Australia. Participants were informed of the methods and study design verbally and in writing before providing a written informed consent.

Experimental Procedures

Participants arrived at the laboratory, having fasted for a minimum of 8 h and abstained from alcohol, caffeine, and vigorous exercise for at least 24 h. Upon arrival, participants were seated and instrumented (approximately 30 min). After this, participants were positioned in a water tank (1.4-m diameter, 1.55-m height, 2386 L) in an upright standing position with their arms resting comfortably on a platform at heart level. The experimental protocol involved two separate 20-min bouts of low-intensity stepping exercise, which consisted of water-based and land-based stepping exercise. These distinct exercise conditions were separated by a 15-min period of land-based seated rest, and the order in which they were performed was randomized between participants. Those participants who were randomly allocated to perform the water-based exercise protocol first were dried with a towel once the tank had been emptied and subsequently covered during the 15-min period of land-based seated rest to prevent reflex thermoregulatory responses. On the basis of the real-time HR and oxygen consumption (V·O2) data, the cadence of stepping exercise was adjusted to match exercise intensity to that observed during the initial exercise bout. We adopted a low-intensity exercise protocol because previous research has demonstrated that mild- to moderate-intensity exercise increases cerebral blood flow by approximately 10%–20% whereas during higher intensities, cerebral blood flow decreases to basal levels (29,31,34). Therefore, we wanted to ensure that the exercise intensity was sufficient to stimulate increases in CBFv in all participants without reaching this threshold. Data were measured and recorded continuously throughout the entire protocol. For every outcome parameter, data were averaged from the last 1–2 min of each 5-min period.

Water-based exercise.

Two submersible water pumps (KPA 600A; Grundfos, South Australia) were placed in an adjacent heated swimming pool. These pumps filled the tank at a constant rate with 30°C water to the level of the right atrium. This process was completed in 9 min. Preliminary experiments indicated that 30°C was consistent with skin temperatures in our young healthy subjects. We also selected this temperature because it is typical of temperatures used in rehabilitation centers, which focus on hydrotherapy. This experimental approach avoided the potential for confounding effects of physical movement into, or out of, the tank on hemodynamics, cutaneous, and CBFv. Once immersed in water, participants remained in the resting upright position for 5 min, which was followed by a 20-min bout of low-intensity exercise consisting of a repetitive stepping protocol (approximately 100 bpm). Upon completion of the exercise bout, participants remained in the resting upright position for a further 5 min, after which, the pumps were reversed to empty the tank.

Land-based exercise.

Participants remained in the upright standing position and avoided movement for 5 min. This was followed by a 20-min bout of low-intensity exercise consisting of a repetitive stepping protocol (approximately 100 bpm). Upon completion of the exercise bout, participants remained in the resting upright position for a further 5 min.

Experimental Measures

Systemic hemodynamics.

A Finometer PRO (Finapres Medical Systems, Amsterdam, the Netherlands) was used to monitor relative changes in MAP, cardiac output (Q·), and stroke volume (SV) via photoplethysmography. These data were exported to a data acquisition system PowerLab (LabChart 7; ADInstruments, Sydney, Australia) in real time. A finger cuff was placed around the middle finger of the left arm, which was supported at right atrium level on a platform. Participants were instructed not to move their arm or finger during recording, and vigilant supervision ensured that this was the case. Total peripheral resistance (TPR) was calculated in real time in LabChart, whereas the cyclical measurement feature used systolic peaks to calculate HR.

MCAv and PCAv.

MCAv and PCAv were measured using a 2-MHz pulsed ST3 transcranial ultrasound system (Spencer Technologies, Seattle, WA). Search techniques adopted to identify the MCA and PCA are described in detail elsewhere (1). Two 2-MHz probes were secured bilaterally at the temporal window with a Marc 600 headframe (Spencer Technologies) to allow for adjustments to the insonation angle until an optimal M-mode image was found. Raw analog MCAv and PCAv traces were exported from PowerLab to LabChart in real time for post hoc analysis.

Oxygen consumption and expired carbon dioxide.

V·O2 and carbon dioxide production were continuously recorded throughout the protocol and calculated from expired gas fractions (Ametek Gas Analysers, Applied Electrochemistry, SOV S-3A/1 and COV CD-3A; Ametek, Pittsburgh, PA) and ventilation (225 A; Morgan, Kent, England) using a metabolic cart. Because of the use of a mixing chamber, all variables were averaged across a 15-s time window; including fractional expired CO2 concentration, which was converted into partial pressure of expired carbon dioxide (PCO2). We did not assess end-tidal CO2 concentrations.

Skin temperature and flux.

Integrated laser Doppler probes (model 413, Periflux 5001 System; Perimed AB, Stockholm, Sweden) were used to continuously monitor skin flux of the forearm and chest (i.e., both measured above the level of water immersion). Skin thermistors were also placed at these sites to assess forearm and chest skin temperature (°C). These data were exported from PowerLab to LabChart in real time. Flux data were converted to cutaneous vascular conductance (CVC), calculated as Flux/MAP (PU mm Hg-1).

Statistics

Analyses were performed using the Statistical Package for Social Sciences for Windows version 21.0 (SPSS, Inc., Chicago, IL). Statistical significance was delimited at P < 0.05, and exact P values are cited (P values of “0.000” provided by the statistics package are reported as “<0.001”). A two-factor (condition vs time) repeated-measures ANOVA was used to compare the effect of water-based exercise with land-based exercise (i.e., “condition”) on hemodynamics and CBFv. Correlation coefficients (two tailed) were used to describe the strength of relations between the change in CBFv and hemodynamic variables across all time points of the water- and land-based exercise protocols relative to resting land-based values. Statistically significant interactions were assessed using the least significant difference approach to multiple comparisons (30). Data are presented mean (95% confidence interval (CI)), unless stated otherwise.

RESULTS

The water- and land-based exercise bouts were successfully matched for V·O2 (13.3 mL·kg-1·min-1 (95% CI, 12.2–14.6) vs 13.5 mL·kg-1·min-1 (95% CI, 12.1–14.8); P = 0.89) (Fig. 1A). HR increased throughout both exercise protocols (P < 0.001); however, we found a significant main effect of water immersion on HR (Fig. 1B). Subsequent pairwise comparisons revealed that HR was significantly lower during water immersion at rest and during recovery but not during exercise (Fig. 1B). V·O2 and HR returned to baseline after 5 min of recovery (P = 0.83 and P = 0.11, respectively).

FIGURE 1.
FIGURE 1.:
Oxygen consumption (V·O2·kg-1·min-1) (A) and HR (bpm) (B) before (“rest”), during (5, 10, 15, and 20 min), and after (“recovery”) a 20-min repetitive stepping land-based ([white circle]) and water immersion (•) exercise bout in 15 healthy participants. Error bars represent SE. P values for the two-way ANOVA data are presented (“time,” “condition,” and “time-condition”). *Indicates P < 0.05 after post hoc analysis when a significant “time-condition” interaction was observed.

Effect of water immersion on CBFv and expired carbon dioxide at rest and during exercise.

MCAv and PCAv increased throughout both exercise protocols (P < 0.001) and returned to baseline after the 5 min recovery period (P = 0.10, P = 0.12 respectively). MCA and PCA blood velocities were elevated during water immersion at rest, throughout exercise and during recovery (Fig. 2A and B). PCO2 increased during both exercise protocols (P < 0.001) and normalized after 5 min recovery (P = 0.96). A significant main effect and time–condition interaction-effect of water immersion was found for PCO2 (Fig. 2C). Post-hoc analysis revealed that PCO2 was significantly elevated during water immersion across all time points of the protocol (Fig. 2C).

FIGURE 2.
FIGURE 2.:
Middle cerebral artery (cm·s-1) (A) and posterior cerebral artery blood velocity (cm·s-1) (B) and PCO2 (mm Hg) (C) before (“rest”), during (5, 10, 15, and 20 min), and after (“recovery”) a 20-min repetitive stepping land-based ([white circle]) and water immersion (•) exercise bout in 15 healthy participants. Error bars represent SE. P values for the two-way ANOVA data are presented (“time,” “condition,” and “time-condition”). *Indicates P < 0.05 after post hoc analysis when a significant “time-condition” interaction was observed.

Effect of water immersion on systemic hemodynamics at rest and during exercise.

SV increased throughout both exercise protocols, and a significant time–condition interaction effect was observed (Fig. 3A). Subsequent post hoc comparisons revealed that water immersion was associated with significantly larger SV at rest and recovery but not during exercise (Fig. 3A). increased during both exercise protocols, but there was no effect of water immersion on the magnitude of increase in (Fig. 3B). MAP was elevated during water immersion at rest, throughout exercise, and during recovery (Fig. 3C). TPR decreased throughout both exercise protocols, and a main effect of water immersion was observed across all time points (Fig. 3D). Finally, we found that SV, , MAP, and TPR all returned to baseline after the 5-min recovery period (P = 0.15, P = 0.10, P = 0.19, and P = 0.33, respectively).

FIGURE 3.
FIGURE 3.:
SV (mL) (A) and (L·min-1) (B), MAP (mm Hg) (C), and TPR (mm Hg·L-1·min-1) (D) before (“rest”), during (5, 10, 15, and 20 min), and after (“recovery”) a 20-min repetitive stepping land-based ([white circle]) and water immersion (•) exercise bout in 15 healthy participants. Error bars represent SE. P values for the two-way ANOVA data are presented (“time,” “condition,” and “time-condition”). *Indicates P < 0.05 after post hoc analysis when a significant “time-condition” interaction was observed.

Effect of water immersion on skin temperature and CVC at rest and during exercise.

We found no effect of exercise or water immersion on the forearm or chest skin temperature (Fig. 4A and B). Forearm and chest CVC increased throughout both exercise protocols (Fig. 4C and D) and returned to baseline after the 5-min recovery period (P = 0.38 and P = 0.43, respectively). Forearm and chest CVC were attenuated during water immersion at rest and throughout exercise (P = 0.03 and P = 0.06, respectively) (Fig. 4C and D).

FIGURE 4.
FIGURE 4.:
Forearm skin temperature (A), chest skin temperature (°C) (B), forearm CVC (C), and chest CVC (D) before (“rest”), during (5, 10, 15, and 20 min), and after (“recovery”) a 20-min repetitive stepping land-based ([white circle]) and water immersion (•) exercise bout in 15 healthy participants. Error bars represent SE. P values for the two-way ANOVA data are presented (“time,” “condition,” and “time-condition”).

Correlations of CBFv.

Changes in MCAv were correlated with changes in PCO2 (r = 0.46, P < 0.001) (Fig. 5) and changes in MAP (r = 0.41, P = 0.004) (Fig. 5) during water exercise. Correlations during land-based exercise ([DELTA]PCO2, r = 0.24 and P = 0.06; [DELTA]MAP, r = 0.25 and P = 0.08) (Fig. 5) were not statistically significant. Similarly, changes in PCAv were correlated with changes in PCO2 (r = 0.27, P = 0.05) and changes in MAP (r = 0.43, P = 0.004) during water-based exercise but not during land-based exercise ([DELTA]PCO2, r = 0.26 and P = 0.06; [DELTA]MAP, r = 0.21 and P = 0.10).

FIGURE 5.
FIGURE 5.:
The relation between [DELTA]MCAv and [DELTA]PCO2 (A) and [DELTA]MAP (B) after water-based (•, solid trend line) ([DELTA]PCO2, r = 0.46 and P < 0.001; [DELTA]MAP, r = 0.41 and P = 0.004) and land-based exercise ([white circle], dotted trend line) ([DELTA]PCO2, r = 0.24 and P = 0.06; [DELTA]MAP, r = 0.25 and P = 0.08).

DISCUSSION

The aim of the present study was to examine whether an acute bout of exercise during water immersion would stimulate greater increases in CBFv than land-based exercise of matched intensity. Our principal finding was that water-based exercise is associated with higher MCAv and PCAv, relative to land-based exercise, in healthy humans.

This study examined acute hemodynamic and cerebrovascular responses to water- and land-based exercise. Importantly, the water- and land-based exercise bouts were successfully matched for V·O2 and HR, indicating that the exercise protocols were of similar relative intensity within subjects and that any observed differences in cerebrovascular and/or hemodynamic responses between exercise bouts were a function of water immersion per se. Participants were immersed in 30°C water to avoid any reflex responses elicited by cold or heat. To this end, we observed no changes in skin temperature during the water immersion period. We suggest that the use of this water temperature allowed for direct and specific examination of the hydrostatic effects of water immersion, but it must be acknowledged that future studies will be required to address the compound effect of exercise performed in warmer or cooler water, which elicits reflex cardiovascular effects.

Previous studies have reported increases in CBFv during mild- to moderate-intensity exercise (29,34,36,43), and we recently demonstrated that water immersion induces increase in MCAv and PCAv at rest (8). In the current study, the increases in CBFv during water immersion at rest persisted throughout exercise and correlated with increases in both MAP and PCO2. This suggests that a summative relation may exist in the contribution of these variables to enhanced CBFv during water-based exercise. Given the complexity of cerebral blood flow regulation during exercise and its multifactorial nature, isolating a sole mediator responsible for the increase in CBFv is problematic but causal relations between MAP, arterial carbon dioxide, and CBFv have been consistently reported (29,31,36). Regardless of the precise mechanism(s) responsible, this is the first experiment to characterize the effect of water immersion during exercise on CBFv in humans.

Our previous report demonstrated that water immersion at temperatures similar to those adopted in the present study elicits increases in MAP and SV and a decrease in HR at rest (8). These findings are consistent with the resting values observed in the subjects recruited for this study. We suggest that increase in central venous pressure and centralization of blood volume associated with water immersion result in increased end-diastolic volume and pressure (5,41). This leads to increase in SV (5,41) via the Frank–Starling effect and consequent decrease in HR. It is noteworthy that the resting differences in SV and HR between water immersion and land were not observed during exercise. This suggests that the effect of hydrostatic pressure is not as prominent during exercise, when venous return is substantially augmented by the muscle pump (32). Indeed, it seems that the action of the muscle pump alone produces an increase in venous return equivalent to that of the muscle pump and hydrostatic pressure combined.

Because HR and SV did not differ between conditions in the present study, we did not observe any differences in Q· during exercise. Although this finding contradicts some previous reports of increased Q· during water immersion at rest (2,5,15) and during exercise (9,37), our observation corroborates other previous work (21,26). The differences between these previous studies with respect to the influence of water immersion on Q· may relate to differences in methodology, particularly water temperature, exercise intensity, and duration of immersion, all of which may elicit reflex changes. In any event, we observed elevated MAP during water immersion at rest and throughout exercise despite the similarity in Q·. This increase in MAP might be related to our finding of elevated TPR in response to water immersion. It is conceivable that water immersion affects cardiopulmonary baroreceptors, with consequent transient changes in sympathetic activity (22,33). Some support for our finding of raised TPR during immersion comes from our data for forearm and chest cutaneous blood flow, measured via laser Doppler flowmetry, which decreased during water immersion. We do not believe that the increased TPR we observed was due to a cold water effect because we went to great lengths to ensure that the water temperature was close to the resting skin temperature in our cohort and because skin temperature did not vary throughout the immersion period.

Although this study benefited from a randomized within-subjects experimental design and contemporary methodology, there are some limitations that warrant consideration. The recruitment of the present study was limited to young healthy volunteers; therefore, we cannot extrapolate these findings to older populations or clinical groups. Secondly, we were unable to directly measure central venous pressure during this study. This may have affected some calculations, such as the TPR values during water immersion. Nonetheless, the consistent temporal nature of the effects and the laser Doppler skin perfusion data suggests that our TPR findings were robust. A final limitation is that we only investigated the effect of low-intensity water-based exercise on CBFv. Given the potential implication that water-based exercise may benefit individuals with cerebrovascular disease, many of whom are elderly and have impaired functional capacity, we wanted to adopt an exercise intensity that potentially could be tolerated by a diverse range of clinical populations. Nevertheless, future studies would benefit from a dose–response assessment of the effects of exercise intensity on CBFv.

Our findings of increased CBFv during water-based exercise raise the possibility of acute and chronic effects of water-based exercise on cerebrovascular function and health. The recurrent episodic increases in blood flow and shear stress that occur as a result of exercise training are potent stimuli for improvement in endothelial function and arterial remodeling in peripheral arteries in humans (18,28,39). Other studies have also suggested that exercise improves cerebrovascular endothelial function by up-regulating endothelial nitric oxide synthase expression through repeated exposure to elevations in blood flow and shear rate (13,17,38). We speculate, on the basis of our findings, that water-based exercise training may induce greater cerebrovascular health benefit than traditional land-based exercise training. However, further research examining the chronic effect of water- versus land-based exercise training on cerebrovascular function and cerebral autoregulation is required to substantiate this claim.

In summary, this is the first study to indicate that water-based exercise induces greater increase in CBFv than land-based exercise of matched intensity. We speculate that water immersion may enhance the recurrent episodic increases in cerebral blood flow and shear stress that occur during exercise and, subsequently, amplify cerebrovascular health benefits associated with exercise training. This study provides a rationale to investigate the therapeutic effect of water-based exercise training on cerebrovascular function and health in humans.

D. J. G. is supported by research funding from the National Health and Medical Research Council of Australia grant (1045204).

None of the authors has declared any conflict of interest.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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Keywords:

CEREBRAL BLOOD FLOW; WATER IMMERSION; EXERCISE; TRANSCRANIAL DOPPLER

© 2015 American College of Sports Medicine