Introduction
Cardiovascular disease remains the number one cause of death in most industrialized
countries [1]. Cardiovascular disease is a cluster of
various types of circulatory diseases affecting the heart and vasculatures. When
breaking it down, the majority of cardiovascular diseases, commonly referred to as
“heart diseases,” are diseases of arteries, as the pathogenesis of
coronary “artery” disease, stroke or cerebrovascular accident, high
blood pressure, and peripheral “artery” disease is attributed to
arterial circulations. Despite this, none of the traditional risk factors for
cardiovascular disease address arterial functions that precede the manifestation of
cardiovascular disease [2]. The vascular system is
critical for health and survival of all tissues and organs, as the vast network
perfuses oxygen and nutrients and eliminates waste products. During exercise, marked
increases in systemic blood flow (i. e. cardiac output) and redistribution
of blood flow are supported by the cushioning or buffering functions of arteries
that are characterized by arterial stiffness [3].
Endothelial function plays a critical role in regulating amounts of perfusion to
various tissues and organs during exercise [4].
Regular physical exercise confers benefits on a number of different diseases and
conditions and acts to reduce overall mortality [5].
One of the most striking conditions on which regular exercise is shown to exert its
influence is cardiovascular disease [6]. The
association of regular physical activity and cardiovascular mortality is well
documented in both observational and longitudinal studies [5]. However, the exact mechanisms underlying the effects of habitual
exercise on cardiovascular disease are currently unknown but have often been
attributed to improvements in cardiovascular risk factors [7]. However, the proportion of the beneficial effects of regular exercise
that can be explained by improvements in cardiovascular risk factors is fairly small
[8]. In one study, >60% of the
variance in coronary heart disease reduction by exercise was not explained by a
comprehensive set of seven traditional risk factors [8]. One of the arguments that has been raised is that improvements in
arterial functions could explain a large remaining proportion of the association
[9]
[10]
[11].
There are a number of arterial functions being measured in clinical and research
settings [12]. The focus of the present review is
placed on two key subclinical markers of vascular diseases: arterial stiffness and
endothelial function. These two functions are also two primary phenotypic features
of vascular aging [11]. Large elastic arteries in
cardiothoracic and carotid regions expand and recoil during cardiac contraction and
relaxation, thereby damping and cushioning fluctuations in arterial pressure and
blood flow. The stiffening of large elastic arteries impairs the buffering function
of the arterial system and leads to cardiovascular dysfunction via a variety of
mechanisms, including elevated systolic blood pressure, augmented left ventricular
afterload, decreased coronary blood flow, and blunting of arterial baroreflex
sensitivity. Indeed stiffness of central elastic arteries is associated with
cardiovascular outcomes above and beyond cardiovascular risk factors [13]. In contrast to central elastic arteries, stiffness
of peripheral muscular arteries (e. g. brachial artery, femoral artery) does
not change with aging or with disease states and does not predict cardiovascular
risks [14]
[15].
Moreover, this segment of arterial stiffness does not appear to change with exercise
training [16]
[17].
Accordingly, clinical and functional significance of peripheral artery stiffness is
currently uncertain.
Endothelium-dependent vasodilation can also be divided into macrovascular (conduit
artery) and microvascular (resistance artery) measures and are typically evaluated
using brachial artery flow-mediated dilation and forearm blood flow responses to
pharmacological stimuli (e. g. acetylcholine and bradykinin) [12] in humans. Interestingly, these two measures of
endothelium-dependent vasodilation are influenced differentially by age and are not
related to one another [18]. Nevertheless, endothelial
function plays a pivotal role in all aspects of atherosclerosis and has predictive
value for future cardiovascular events [19]. The
amount of available studies on venous function is extremely limited and not included
in the present review. However, there is experimental evidence indicating that
venous compliance in legs is greater in endurance-trained adults than in sedentary
adults [20] and increases with endurance training
interventions [21].
Various forms of exercise intervention have been conducted and evaluated to reduce
risks of cardiovascular disease. Most of the available studies to date have
addressed effects of walking and running as an aerobic exercise and weight training
as a form of resistance training on vascular functions. A number of review papers
have been written and are available in the literature to emphasize the benefits or
a
lack thereof of these traditional or main stream exercises on the vasculature [9]
[10]
[11]. However, exercises and sporting activities are
extremely diverse, as a substantial variation is introduced every time it is
practiced in different media (water, land or snow), seasons (winter or summer), and
settings (individual, pair, group or team) ([Fig.
1]).
Fig. 1 Influence of a variety of exercises and sporting activities on
vascular function.
A myriad of choices among various modes of exercise to target vascular dysfunction
may be analogous to pharmacological treatments for hypertension. There are a total
of six different classes of antihypertensive drugs being used clinically [22]. Even though the initial treatment strategy is
diuretics for most, clinicians are advised to change the choice of drugs depending
on a number of conditions including coexisting disease, race, and side effects [23]. Even within the class of diuretics, there are
multiple choices of drugs to select. As a choice of proper drug is critically
important to elucidate the best possible clinical outcome, a selection of proper and
preferred exercise mode that can be adhered to is equally important to enhance the
effectiveness of exercise programs. Participants assigned to aerobic exercise class
that matched their preferred choice had better attendance and expressed a greater
intention to continue exercising than those assigned to the standard exercise class
[24]. If walking or running is not a preferred
mode of exercise, which activity will be selected as a primary form of exercise? If
the overall exercise program is to be diversified to reduce boredom and enhance
enjoyment, as well as to accommodate exercise tolerance, what other activity can be
chosen to reduce cardiovascular risks? More importantly, investigators and
clinicians should be aware of the research evidence for a variety of exercises used
to enhance vascular functions.
In this review, four categories of exercises and sports that have been
under-appreciated and overlooked are highlighted ([Fig.
1]). They include water-based exercises (swimming, aquatic exercise,
rowing), mind-body interaction exercises (yoga, Tai Chi, walking meditation), ball
sports (soccer, football), and winter sports (Alpine skiing). For the purpose of
this review, only investigations that reported arterial stiffness and endothelial
function as outcome measures are included in the review.
Swimming
Swimming is one of the most popular forms of physical activity, and is often
included as a recommended mode of exercise for overall health and fitness [25]. Similar to walking and cycling, it is a
dynamic rhythmic aerobic exercise that involves a large muscle mass [26]. But swimming is substantially different as a
mode of exercise. It is performed in a different medium than
walking/running (i. e. water) and in the supine/prone,
rather than the upright posture, resulting in a zero-gravity situation. Because
of its non-weight-bearing nature, swimming has a much lower rate of orthopedic
injury than does running [27]. Indeed swimming
appears to be an excellent form of exercise for patients with osteoarthritis
[28]. Due to decreased heat load resulting
from high thermoconductivity of water, risks of heat exertion that obese adults
often experience are reduced substantially. Unlike other popular modes of
exercises (e. g. walking, cycling), swimming is a full-body task that
the majority of the propulsive force comes primarily from upper body [29]. As differences in vasodilatory responses have
been reported between arms and legs [30], arterial
adaptations may be different between swimming and land-based exercises. From the
exercise prescription standpoint, swimming can be an ideal form of exercise,
particularly for elderly patients, obese patients, patients with arthritis, and
those who have problems and tolerance issues with weight-bearing activities. In
spite of the fact that swimming is one of the most popular, most practiced and
most prescribed modes of exercise, surprisingly little research-related
information is available regarding the influence of regular swimming on
cardiovascular risks [25].
In a cross-sectional study, middle-aged and older swimmers demonstrate reduced
levels of arterial stiffness than sedentary peers and a similar level of
arterial stiffness to runners who are matched for weekly training volume [31]. However, brachial artery flow-mediated
dilation of swimmers is similar to sedentary peers and lower than runners [31]. This particular finding seems strange at first
glance as the major working muscles in swimming are arms on which flow-mediated
dilation was measured. From the standpoint of redistribution of blood flow
during exercise, blood flow to non-working muscles (arms) is thought to be
reduced [32]. However, substantial increases in
arm blood flow have been observed during leg cycling exercise [33].
In an exercise intervention study involving older patients with osteoarthritis,
swimming training performed at moderate intensity reduced central arterial
stiffness as assessed by carotid-femoral pulse wave velocity and increased
endothelium-dependent vasodilation as evaluated by brachial artery flow-mediated
dilation [34]. Cycling training, which was
implemented as a non-weight bearing land-based comparison group, decreased
arterial stiffness but did not change endothelium-dependent vasodilation [34]. Physiological mechanisms underlying the impact
of swimming training on vascular function is not known. But in an animal study,
reductions in arterial stiffness induced by swimming exercise are associated
with the corresponding changes in eNOS phosphorylation [35].
In a clinical trial involving older patients with essential hypertension, three
months of swimming intervention performed at moderate intensity not only reduced
ambulatory and central blood pressure but also improved endothelium-dependent
vasodilation and central arterial stiffness [36].
This finding is particularly noteworthy because walking-based exercise
interventions have not been shown to be effective as destiffening therapy for
older patients with essential hypertension and diabetes [37]
[38]
[39]. Taken together, the available evidence indicates that swimming
is an excellent form of exercise to improve vascular functions in older adults
with and without existing clinical conditions.
Aquatic exercise
Swimming is an excellent mode of physical activity. However, it requires adequate
skills and techniques to achieve target exercise intensity during exercise. As
such, some individuals cannot initiate the exercise program right away. Aquatic
exercise is an alternative water-based exercise that most people can begin to
engage without any special skills and techniques. Does aquatic exercise
performed in shallow water in the upright posture produce similarly beneficial
impact on vascular functions to swimming? Ten weeks of aquatic exercise reduces
aortic pulse wave velocity in older adults [40].
In patients with type 2 diabetes, an improvement in flow-mediated dilation has
been observed after eight weeks of aquatic exercise performed at a moderate
intensity [41]. Thus, the available studies,
though limited in numbers, are consistent with the notion that aquatic exercise
is beneficial in improving vascular functions.
Considering that both swimming and aquatic exercise exert favorable influence on
the vasculature, could at least some portion of the favorable influence be
attributed to water immersion? Interestingly, there are many investigations
indicating that exercises performed in water are more effective in improving
vascular function than the same exercises performed on land. For example, in
older patients with type 2 diabetes, land-based and water-based moderate cycling
exercise performed three times a week for 12 weeks produced significant
increases in flow-mediated dilation in the popliteal artery and decreases in
arterial stiffness [42]. However, indices of
cutaneous macrovascular reactivity as assessed by post-occlusive reactive
hyperemia improved only in the water-based exercise group [42]. The reason for the relative efficacy of
water-based vs. land-based exercises is not clear. However, there is an
experimental evidence indicating that circulating levels of nitric oxide
metabolites increased after water-based exercise but not after same exercise on
land in patients with heart disease [43].
Similarly, skeletal muscle nitric oxide synthase content was increased after 12
weeks of aquatic treadmill exercise but not after treadmill exercise performed
on land [44]. Plasma and blood volume can exert
marked influences on blood pressure and vascular function. Plasma volume
expansion that occurs with exercise appears to be smaller in swimmers than in
runners [45].
Rowing
Theoretically, rowing is an outstanding form of exercise that is low impact and
dynamic in nature and involves a large muscle mass. Rowing is also a
time-efficient mode of exercise as it simultaneously involves components of both
aerobic endurance and muscular strength as demonstrated by rowers’ large
aerobic capacity and muscle strength [46]. In an
cross-sectional study, central arterial compliance is greater and beta-stiffness
index is lower in habitual rowers than in age-matched sedentary controls [16]. The reduced arterial stiffness in rowers is
associated with a greater cardiovagal baroreflex sensitivity [16].
In a study of young elite rowers, brachial artery flow-mediated dilation assessed
by MRI was not different between rowers and sedentary controls [47]. Interestingly, endothelium-independent
vasodilation as assessed by nitroglycerine administration was significantly
lower in rowers than in sedentary controls [47].
There is also a report of no differences in plasma nitrite and nitrate and
endothelin-1 levels between older habitual rowers and sedentary controls [48]. Physiological explanations for these findings
are not clear. But it could be interpreted as habitual rowing producing smooth
muscle cell desensitization. We were not able to locate clinical trials or
randomized control trial involving rowing training on vascular function.
Mind-body interaction exercises
Mind-body medicine in the form of meditation, relaxation and prayer has become
popular in recent decades for the strategies to manage psychological stress and
improve overall health [49]
[50]. To augment its effect, it can be incorporated
and combined into a form of exercise including yoga and Tai Chi. A number of
other forms of mind-body interaction exercises (e. g. laughter yoga,
Buddhist walking meditation) have also been studied actively [51]
[52].
Tai Chi is an ancient Chinese callisthenic exercise and martial art that combines
a series of slow, relaxed and graceful movements with deep breathing techniques.
In an observational study, older practitioners of Tai Chi demonstrated enhanced
endothelium-dependent vasodilation in the skin vasculature as assessed by
changes in laser Doppler flow in response to iontophorertic infusion of
acetylcholine [53]. Additionally, in older
patients with peripheral neuropathy, progressive Tai Chi practiced three times a
week for 12 weeks produced a 25% increase in vascular reactivity index
measured by fingertip digital thermal monitoring [54]. In a randomized control trial that compared 16 weeks of Tai Chi
training and an educational program, elderly women assigned to Tai Chi were able
to improve both large artery and small artery compliance as assessed by the HDI
device [55]. Thus, there is sufficient evidence to
indicate that Tai Chi is effective in improving vascular function.
Walking meditation or mindful walking is a widely practiced form of Buddhist
practice that focuses on mind-body interactions. It incorporates the principles
of traditional meditation performed in the sitting position, including
breathing, awareness, concentration and relaxation, with rhythmic exercise of
walking [52]. In a clinical trial investigating
the comparative effects of Buddhist walking meditation and traditional walking
in middle-aged and older patients with type 2 diabetes, flow-mediated dilation
increased significantly in both training groups [56]. However, a reduction in arterial stiffness, as well as a
decrease in hemoglobin A1c, were observed only in the Buddhist walking
meditation group. These results suggest that spirituality-based exercise program
is effective in producing a multitude of health benefits relevant to middle-aged
and older patients with type 2 diabetes.
Yoga
Yoga is a practice that has been performed over 5,000 years in the Eastern part
of the world, and it has become increasingly popular as a mode of exercise in
the Western part of the world. Yoga is an attractive form of exercise from the
vascular health standpoint when it is broken down into its elements
(e. g. stretching, static exercise and meditation) [57]. One primary physical component of yoga is
stretching. An inverse association has been reported between trunk flexibility
and arterial stiffness [58]
[59]. Stretching intervention has been shown to
reduce arterial stiffness in previously sedentary adults [60]. Additionally, even though a variety of yoga
postures evoke significant increases in blood pressure [59], yoga postures are characterized by static or isometric exercises
that could act to reduce blood pressure and improve endothelial function [61]. Moreover, meditation incorporated in yoga
could improve vascular function presumably through reductions in sympathetic
vasoconstrictor tone [62].
In a cross-sectional study comparing yoga practitioners and sedentary peers, no
significant differences were found in central arterial stiffness and brachial
artery flow-mediated dilation [63]. Twelve weeks
of yoga practices did not change arterial stiffness and flow-mediated dilation
in previously sedentary middle-aged adults [63]. A
lack of effects of yoga does not appear to be an issue of short intervention
length, as eight months of yoga intervention also fails to reduce arterial
stiffness in middle-aged premenopausal women [64].
In contrast, a study in India compared yoga and brisk walking performed for
1 h six days a week for 12 weeks, and found that arterial stiffness was
significantly reduced with yoga but not with brisk walking in elderly
participants with elevated blood pressure [65].
Compared with regular or traditional yoga (e. g. hatha yoga), there is
more evidence indicating the benefits of Bikram yoga, a highly standardized
rigorous yoga of 26 postures practiced in a heated environment with
40–60% relative humidity. A relatively short-term practice of
Bikram yoga improved brachial artery flow-mediated dilation [66] and central arterial stiffness [67] although the effects seem to be modulated by
age. Given the observations that both sauna [68]
and hot water immersion [69] have been shown to
improve vascular function, it seems reasonable to attribute the superior effects
of Bikram yoga to the heated practice environment. However, the magnitude of
improvements in endothelium-dependent vasodilation appears to be similar between
Bikram yoga performed in the thermoneutral environment and hot humid environment
[70].
Ball sports
Association football, more commonly referred to as soccer or football, is the
most popular sport in the world. The playing style touches on many elements of
overall physical fitness and can be considered as a form of high-intensity
interval training incorporated into a ball game. Since it is played as a team
with teammates, it is perceived as more motivating and enjoyable than individual
exercise or sport [71]. A cross-sectional study
demonstrated that older soccer players show more favorable endothelial function
as measured by peripheral artery tonometry [72].
However, an exercise intervention study conducted by the same group is not
consistent with the cross-sectional study. Twelve months of soccer training did
not change endothelium-dependent vasodilation in older men although the overall
cardiovascular benefits were confirmed by significant increases in maximal
oxygen consumption [73]. In another intervention
study in middle-aged men with hypertension, six months of soccer training
performed twice a week reduced augmentation index [74], an index of arterial wave reflection that is indirectly
associated with arterial stiffness. Given a small number of studies relative to
the popularity of soccer, a lot more studies are needed to determine its
vascular effects.
American-style football is the most popular spectator sport in the United States.
American football has spread all over the world, as American football
federations are present on most continents. Unlike other ball sports, this team
sport is not widely practiced by middle-aged and older populations. However,
non-contact variants of American football, including flag football and touch
football, are practiced by youths, coeds and older adults. In collegiate
football athletes, arterial stiffness increases significantly from a preseason
to the end of a single season of football [75].
Additionally, arterial stiffness measured in the pre-season increases gradually
year after year during the college football players’ careers [76]. A key component of the overall training
regimen in American-style football is strenuous resistance training. Resistance
training has been demonstrated to increase arterial stiffness in young and
middle-aged adults [77]
[78]
[79]. Stiffening effects of
resistance training have also been observed in resistance training performed at
a moderate intensity [80]. In studies involving
older adults, resistance training does not appear to elevate arterial stiffness
possibly due to the high baseline arterial stiffness causing a ceiling effect
[60]
[81].
Information regarding the effects of other ball sports on vascular function is
very limited. For instance, tennis players are frequently-used experimental
model of investigating dominant (active) and non-dominant (relatively inactive)
limbs [82]
[83]
[84]. However, there have not been any randomized
clinical trials or exercise interventions that addressed the effects of tennis
practices on vascular function. Ball sports are extremely diverse in nature. A
variety of ball sports including basketball and volleyball are practiced and
enjoyed by youths and adults varying widely in age. More research emphasis
should be devoted to these overlooked ball sports.
Winter sports
Winter sports are sports or recreational activities that are performed on snow or
ice. Among them, Alpine skiing is practiced widely in mountainous regions that
receive adequate amounts of snowfall in the winter. It is the most popular
winter sport world-wide, and over a million people enjoy Alpine skiing in
Austria alone. From the physiological standpoint, Alpine skiing can be
considered a form of interval training as hard work on downhill slope that could
stress both muscular strength and cardiovascular fitness is interspersed by
respites on the chairlift or gondola. In a study involving older healthy adults
who were either beginners or intermediate levels of Alpine skiing at the
beginning of the study, 12 weeks of Alpine skiing did not alter circulating
biomarkers of endothelial function and inflammation [85]. In a follow-up study [86],
circulating biomarkers of endothelial function did not change once again.
Additionally, the reactive hyperemia index did not change in the intervention
group although early, but not late, endothelial progenitor cells increased [86]. Thus, the currently available information does
not seem to support the notion that Alpine skiing exerts beneficial impact on
endothelial function. We were not able to find clinical trials evaluating Alpine
skiing or other winter sports on arterial stiffness. Even though a variety of
other winter sports, including cross-country skiing, snow shoeing, ice climbing
and curling are widely practiced and enjoyed recreationally, their impacts on
vascular health are largely unknown.
Perspective
In spite of the fact that the modes of exercise and sports that individuals can
select and engage in are numerous, most of the available research studies have
focused on the mainstream exercises such as walking/running and
resistance/weight training. There are a number of under-emphasized and
overlooked exercises that can exert beneficial impacts on key vascular
functions. For some exercises (e. g. archery, tennis), no research has
been conducted to determine their efficacy. In real life situations, exercise is
a part of the overall lifestyle modifications and often combines with other
interventions. However, additive or synergistic effect of exercise combined with
other lifestyle modifications are largely unknown. Individuals are advised to
diversify exercise routines to reduce boredom and enhance enjoyment but the
effects of “cross-training” that combine multiple modes of
exercise have not been studied adequately [87].
Appreciation of the effects of under-appreciated and overlooked modes of
exercise is critical, as the exercise prescription can be tailored or
personalized to maximize the effectiveness of exercise therapy. Clearly, a lot
more research on vascular function is warranted to line up as many exercise
modes as we can for the “exercise is medicine” arsenal.
