Medicine & Science in Sports & Exercise:
Aortic Stiffness Increased in Spinal Cord Injury When Matched for Physical Activity
PHILLIPS, AARON A.1,2,4; COTE, ANITA T.1,3; BREDIN, SHANNON S. D.3; KRASSIOUKOV, ANDREI V.4,5; WARBURTON, DARREN E. R.1,2,4
1Cardiovascular Physiology and Rehabilitation Laboratory, Physical Activity Promotion and Chronic Disease Prevention Unit, University of British Columbia, Vancouver, CANADA; 2Experimental Medicine Program, Faculty of Medicine, University of British Columbia, Vancouver, CANADA; 3Cognitive and Functional Learning Laboratory, University of British Columbia, CANADA; 4International Collaboration of Repair Discoveries, University of British Columbia, Vancouver, British Columbia, CANADA; and 5Division of Physical Medicine and Rehabilitation, Department of Medicine, University of British Columbia, Vancouver, British Columbia, CANADA
Address for correspondence: Darren E. R. Warburton, Ph.D., University of British Columbia, Rm. 205, Unit II Osborne Centre, 6108 Thunderbird Blvd, Vancouver, BC, Canada V6T 1Z3; E-mail: email@example.com.
Submitted for publication February 2012.
Accepted for publication June 2012.
Purpose: The objective of this study is to compare arterial stiffness between those with spinal cord injury (SCI) and able-bodied (AB) individuals when matched for habitual level of physical activity.
Methods: A total of 17 SCI and 17 AB individuals were matched for sex, age, weight, blood pressure, and levels of self-reported habitual physical activity (Godin–Shephard). Measures included central pulse wave velocity (PWV) (carotid–femoral PWV (cfPWV)) and lower limb PWV (femoral-–toe PWV(ftPWV)) as well as large and small arterial compliance.
Results: The cfPWV was significantly elevated (7.3 ± 2.1 vs. 5.7 ± 1.4 m·s−1, P < 0.05) in SCI compared with AB. No other measures of arterial stiffness were different between the groups. Moderate to vigorous physical activity was significantly correlated with both large (r = 0.48, P < 0.05) and small (r = 0.65, P < 0.01) artery compliance, but not cfPWV or ftPWV.
Conclusions: Both large and small artery compliance appear to be associated with habitual physical activity in physically active individuals with SCI. However, we did not show that physical activity is associated with PWV in physically active individuals with SCI. These findings suggest that factors other than physical inactivity may mediate the increase in arterial stiffness widely reported in the SCI population.
It is well established that increasing vascular stiffness is associated with an increased risk of cardiovascular disease (CVD) in the able-bodied (AB) population (23). An elastic vascular system reduces cardiac demand (1), increases coronary artery perfusion (18), and is related to reduced atherosclerotic progression (20). Arterial compliance and pulse wave velocity (PWV) are common established markers of vascular stiffness (4,22), with the latter being considered the gold standard (22). Both peripheral and central arterial stiffness appear to be increased in CVD, although central PWV has been shown to be more strongly correlated to CVD (34). Furthermore, a recent systematic review has shown increasing central PWV to be highly predictive of both cardiovascular morbidity and all-cause mortality (36).
Only recently, we have become aware that CVD is the primary cause of mortality in the chronic phase of spinal cord injury (SCI) (12). Those with SCI are at an elevated risk for CVD as compared with the AB population (7,38). A pilot study has reported increased central PWV in SCI as compared with AB (25); however, those with SCI are physically inactive compared with the AB population (15). Also, detrimental changes in carbohydrate and lipid metabolism occur after SCI (5). This may result in differential stiffening of peripheral arterial segments because the periphery has been shown more sensitive to lipid changes than central arterial segments (34). Because physical activity is strongly associated with improved central arterial stiffness and reduced CVD risk in AB individuals (37), it is unclear if increased arterial stiffness in the SCI population is due to reduced physical activity or other factors. In our recent systematic review, we showed that exercise is an effective therapeutic tool for improving both central and peripheral vascular health in those with SCI (30). One recent study found no difference in arterial stiffness between wheelchair athletes with SCI and age-matched controls; however, this article did not quantify physical activity levels, examined only central arterial stiffness, and used less established markers of arterial stiffness (17). We have also demonstrated that persons living with SCI have reduced small artery compliance in comparison with AB controls (39). Moreover, three articles, including one by our group, have revealed that physical activity appears to offset the decline in small artery and peripheral compliance seen with SCI (6,8,39). However, little is known about the effects of physical activity on both central distensibility and compliance in SCI, which provide different information on arterial function. Compliance relates to arterial capacitance, whereas distensibility is associated more with the elastic arterial properties (27). Accordingly, a more comprehensive examination of the relationship between exercise and arterial stiffness in SCI is required.
The purpose of the present study is to compare well-established measures of arterial stiffness, from both central and peripheral segments, between those with SCI and non-SCI controls when quantitatively matched for physical levels. Furthermore, because injuries above the sixth thoracic spinal segment often result in marked affects on cardiovascular autonomic control (19), we also aimed to compare arterial stiffness parameters in those with high versus low injuries to the spinal cord. We hypothesized that two populations will have comparable vascular stiffness profiles when matched for physical activity levels.
Seventeen individuals with SCI (C5–L3, ASIA A, B, and C) participated in this study (SCI) (Table 1). All participants were at least 1 yr postinjury (12 ± 8 yr). The control group was composed of 17 participants matched for age and sex (AB). Participants from the SCI group were recruited through posters placed at the Blusson Spinal Cord Centre of the International Collaboration on Repair Discoveries and through several local wheelchair sport organizations. AB participants were recruited from posters placed around the University of British Columbia campus. Participant characteristics are presented in Table 2.
All participants were instructed to abstain from caffeine, exercise, and alcohol for 24 h before testing. Those who were smokers or had any history of CVD were excluded from participation. All participants provided written informed consent in accord with the Clinical Research Ethics Board at the University of British Columbia, who approved this study.
After arriving to the laboratory, all participants completed a questionnaire regarding leisure time physical activity (Godin–Shephard Leisure Time Physical Activity Questionnaire). Matching physical activity in the SCI population to AB is difficult. For example, maximal aerobic power (V˙O2max), which is the measure used to establish the validity of physical activity questionnaires, is extremely difficult to match between AB individuals and SCI (16). It could be argued that an electronic device motion sensor (such as an accelerometer) should be used for matching AB and SCI for physical activity levels. Typically, this may be a valid concern in studies of SCI, given their inactive lifestyle and the fact that the main shortcoming of self-report physical activity measures is a floor effect where the minimum physical activity level is actually too high for inactive individuals (35). Because our SCI population was highly active, self-report is an accurate tool for measuring physical activity levels. Furthermore, the Godin–Shephard tool has been used in several studies assessing physical activity levels in those with SCI (21,28). As per Godin’s guidelines (13), only units of moderate and vigorous physical activity (MVPA) were evaluated in relationship to measures of arterial stiffness.
After completion of the physical activity questionnaire, participants were positioned supine on a dedicated research bed. Blood pressure (BP) was measured using an automated cuff (BpTRU-BPM-100, Coquitlam; VSM Medical, Vancouver, BC, Canada) after 5 min of supine rest. Four consecutive BP and HR measures separated by at least 1 min were averaged. After BP measurements, arterial compliance was measured noninvasively via applanation tonometry (HDI CR-2000; Hypertension Diagnostics, Eagan, MN) for diastolic pulse contour analysis, which was then incorporated into a modified Windkessel model of circulation. This model considers the arterial tree loaded by stroke volume during systole, whereas the diastolic decay contour is considered a function of resistance, compliance, and inertance of an isolated arterial system. Large-capacitive arterial compliance (Comp1) is derived from more proximal arterial segments and depends on arterial caliber. However, small-oscillatory (Comp2) compliance is derived from the frequency and diastolic decay rate of pressure waves created at downstream sites of reflection. Oscillatory compliance is dependent on both the elastic and geometric properties of the large arteries as well as pulse wave reflections (27). After stabilizing the wrist and maximizing signal strength, radial artery tonometry measurements were collected using the right wrist while at the same time an automated BP cuff was affixed to the upper left arm. Thirty-second measurements were taken in duplicate and analyzed for analysis.
Immediately after arterial compliance measurements, pulse wave contours were collected on Chart (version 5.5.6, ADInstruments, Colorado Springs, CO) at the carotid artery, femoral artery, and toe using infrared photoelectric sensors (ADInstruments, Colorado Springs, CO). A single investigator collected a minimum of 30 consecutive cardiac cycles, which were averaged to calculate the foot-to-foot pulse transit time between the carotid artery and femoral artery, as well as the femoral artery to toe. The foot of the wave, identified as the last point before a sustained increase in pressure (the upstroke), was automatically detected with a specifically designed automated program. The shortest distances between the sites of pulse contour collection were measured to the nearest 0.5 cm using a standard measuring tape. The segmental distances were divided by the corresponding pulse transit time to calculate PWV between 1) the carotid artery and femoral artery (cfPWV) and 2) the femoral artery and toe (ftPWV). The same investigator (AP) recorded and analyzed all arterial pressure wave forms and segment distances. While analyzing PWV files, the investigator was blinded to the subject ID as well as subject group (i.e., SCI or AB). Within our laboratory, using these techniques and a “plethysmograph to plethysmograph” signal, we have documented a high cfPWV repeatability (coefficient of variation = 5.5%). Similar coefficients of variation have been documented in our laboratory for ftPWV (3.9%).
Cardiovascular variables were compared between SCI and AB using independent-samples t-tests. Bivariate linear correlations were performed to evaluate the relationship between PWV and MVPA, age, and years since injury. The level of significance was set a priori at P < 0.05. Data are presented as mean ± SD. Data analysis was performed using SPSS 16.0 (SPSS, Chicago, IL).
Participants were matched for age, MVPA, sex, and body mass. In those with SCI, systolic BP (SBP), diastolic BP (DBP), and mean arterial BP (MAP) were all significantly lower than reported in AB (Table 2). Central PWV was significantly increased in SCI as compared with AB controls. No other measure of arterial stiffness was different between groups (Table 3). Correlations between various cardiovascular and possible influencing factors are presented in Table 4. Both Comp1 and Comp2 were significantly correlated with MVPA within our SCI group (Fig. 1). No significant correlation was found between any arterial stiffness measure and sex or level of injury. There was also no significant difference found between those with injuries below T6 as compared with those with injuries T6 and above for cfPWV (7.0 ± 2.2 vs. 7.9 ± 1.7 m·s−1 ), ftPWV (9.4 ± 2.4 vs. 10.8 ± 3.5 m·s−1), Comp2 (8.3 ± 3.0 vs. 10.4 ± 3.3 mL·mm Hg−1 × 10), or Comp1 (19.5 ± 3.1 vs. 17.5 ± 4.0 mL·mm Hg−1 × 10). BP was on average lower in those with SCI above the sixth thoracic spinal segment; however, this difference was not statistically significant (SBP, 110 ± 11 vs. 117 ± 8 mm Hg; DBP, 59 ± 9 vs. 63 ± 8 mm Hg; 76 ± 9 vs. 81 ± 8 mm Hg).
Our present investigation has revealed several important and novel findings. In this sample of 17 individuals with SCI, we have shown that central but not lower limb arterial stiffness is reduced when compared with age, sex, body mass, and physical activity–matched AB controls. Also, we have illustrated that increased MVPA is associated with improved small and large artery compliance but not central PWV within the SCI population. These findings have important implications for the prevention of CVD and quality of life in SCI.
Our central PWV values are somewhat low considering previous work in both SCI and healthy AB individuals (25). However, these findings are consistent with the literature given the comparatively young and highly active population we chose to examine. For instance, by the standards outlined by Godin (13), 15 of 17 SCI and 14 of 17 AB were considered highly active by their level of self-reported MVPA. Also, our SCI population is on average 10 yr younger than prior work examining PWV in SCI (25). Our results are in line with PWV values reported for similar aged participants (24) and highlight that physically active individuals with and without SCI have central PWV below the threshold level associated with increased risk of CAD (13 m·s−1) as described by Blacher et al. (2).
Miyatani et al. (25) have shown that central but not peripheral PWV is increased in an age-, sex-, height-, and weight-matched sample of those with SCI. Our work extends these findings by suggesting that SCI-related increases in arterial stiffness may not be fully explained by differences in physical activity levels. Two studies have measured the relationship between physical activity and arterial stiffness in those with SCI (17). One study, by Tordi et al. (33), reported that a single individual had improved arterial stiffness after 6 wk of interval training. It is difficult to compare our results, which matched individuals on their habitual physical activity, with those of Tordi who reported the response of a single individual to a highly specific and intense exercise regimen (17). Our research group also recently revealed that small and large artery compliance were similar in physically active SCI individuals (i.e., individuals meeting the minimal recommendations for health benefits) in comparison with active AB counterparts, whereas inactive participants had markedly lower small artery compliance, supporting further the influence of physical activity on arterial compliance in both SCI and AB populations (39).
Another study evaluating exercise and arterial stiffness supports our finding that arterial compliance is similar between SCI and AB when controlling for physical activity; however, it also showed that other markers of central arterial stiffness, namely, beta stiffness index of the carotid artery, were similar between groups (33). Because prior research has clearly shown that stiffness of the carotid artery is less sensitive to atherosclerotic risk factors than the aorta (29), we have examined more closely central arterial stiffness in physical activity–matched SCI. In light of our findings, it is reasonable to suspect that factors other than habitual exercise are responsible for central arterial stiffening in those with SCI. After SCI, both glucose tolerance and sympathetic regulation of arterial tone are affected detrimentally (9,31), both of which have been shown to negatively affect arterial health (9,11,14). Glucose tolerance may be affected by physical activity levels; however, evidence suggests that the loss of leg muscle mass after SCI may also affect negatively glucose metabolism (10). It is plausible that the loss of leg mass and glucose tolerance after SCI may lead to more pronounced changes in arterial stiffness over the lifespan, even when matched for physical activity with AB individuals.
The Bramwell–Hill equation relates PWV inversely to distensibility (3). Accordingly, PWV is less affected by resting diameter as compared with arterial compliance and therefore more directly estimates arterial stiffness (27). Furthermore, the Windkessel modeled estimates of compliance are measures of arterial capacitance (27). Perhaps because of this fundamental difference between measures, poor agreement has been shown between central PWV and both small and large artery compliance (40). This important distinction is often neglected in clinical literature where the terms arterial distensibility and compliance are used somewhat interchangeably. As our work shows that compliance is not different between SCI and AB when matched for physical activity, as well as a moderate association between MVPA and compliance, it is likely that physical activity may predominantly influence the systemic capacitance properties of arteries, but not stiffening itself, within the SCI population. A couple of potential mechanisms may explain similar systemic large and small artery compliance between AB and SCI when matched for physical activity. First, as increased diameter is a sufficient factor to improve compliance, work by Nash et al. (26) provides an explanation for the findings of our study by showing that tetraplegics who habitually exercise have significantly larger common femoral artery cross-sectional area as compared with sedentary tetraplegics (and similar to AB). In some contrast to this theory, however, there are two studies showing that arterial compliance is improved in the lower limb after exercise without concomitant increases in diastolic cross-sectional area. These articles both used specialized exercise programs designed to mobilize the lower limbs, either through body-weight-supported treadmill training or functional electrical stimulation (6,8). As such, these experiments do not directly compare with the current study, which examined habitual physical activity primarily associated with upper arm operation of a wheelchair. Second, wheelchair athletes typically perform primarily upper body exercise, and Shenberger et al. (32) have shown that chronic upper body exercise led to increased upper body arterial diameter in SCI as compared with AB controls. This improvement in upper body vascular capaciance may mathematically compensate for decreases in compliance seen centrally, causing a normalization of systemic indicators of compliance, as measured in our study.
We also did not report a significant difference in lower limb PWV between SCI and AB, which is consistent with the work by Miyatani et al. (25) that reported no difference between SCI and AB. However, the findings of our work are unique in that the SCI population was matched for physical activity levels in addition to age, sex, and body mass (key determinants of vascular health). It deserves mention that the clinical value of this measure has recently come into question, because central PWV has been shown to be more sensitive than peripheral PWV to changes associated with CAD, cerebrovascular disease, and even peripheral artery disease (34).
Our study has several considerations that deserve discussion. First, it is known that mean arterial pressure can influence arterial stiffness according to the nonlinear relationship between arterial distension and stiffness (27). We chose not to statistically control for the interaction of mean arterial pressure because it was not significantly associated with either central or lower limb PWV (Table 4). Second, the cross-sectional design of this study, which examines a single point in time with the aim of comparing populations, precludes determining cause and effect. A longitudinal study that follows participants for a number of years would better describe the “dose response” of physical activity on arterial properties in SCI. We also reported a significant correlation between both small and large artery compliance with age, sex, and HR. This is likely due to age, HR, and sex being used to estimate cardiac output, which in turn is used to calculate total peripheral resistance and therefore both Comp1 and Comp2 through the modified Windkessel model used by the compliance measuring device used in this study. Finally, although pulse contour analysis for estimating compliance has not been directly validated for the SCI population, it has been widely used in a number of studies examining arterial patterns in SCI (30).
A number of important studies should be completed to further examine our findings. An interesting future direction of this line of research would include using a group of participants who have performed long-term leg functional electrical stimulation exercise compared with a group of upper body athletes, in an attempt to highlight the role glucose metabolism has on central PWV. Also, it would be interesting to compare SCI participants with and without intact sympathetic control of the aorta due to injury level.
The results of our study demonstrate those with SCI have increased central arterial stiffness when compared with age, sex, body mass, and physical activity level–matched AB individuals. Furthermore, regular participation in physical activity may differentially influence compliance (stiffness and capacitance) and PWV (stiffness) in those living with SCI. When considering prior work using similar study design, this finding highlights the importance of using a variety of indicators of stiffness when aiming to quantify arterial health in the SCI population.
This research was supported by funding from the Canadian Institutes of Health Research, the Michael Smith Foundation for Health Research, the Natural Sciences and Engineering Research Council of Canada, the Canada Foundation for Innovation, and the BC Knowledge Development Fund. AA Phillips was supported by scholarships from Mathematics of Information Technology and Complex Systems (Canada), the Natural Sciences and Engineering Research Council of Canada, and The University of British Columbia Faculty of Medicine. DER Warburton was supported by salary awards from the Canadian Institutes of Health Research and the Michael Smith Foundation for Health Research.
Special recognition is given to the athletes of the Vancouver 2010 Paralympics as well as the British Columbia Wheelchair Sports and Disabled Skiers Associations of British Columbia.
The authors declare no conflicts of interest.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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