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Original Research

Sexual Dimorphism in the Estimation of Upper-Limb Blood Flow Restriction in the Seated Position

Borges, Afonso1; Teodósio, Carolina1; Matos, Pedro1; Mil-Homens, Pedro1,2; Pezarat-Correia, Pedro1,2; Fahs, Christopher3; Mendonca, Goncalo V.1,2

Author Information
Journal of Strength and Conditioning Research: July 2018 - Volume 32 - Issue 7 - p 2096-2102
doi: 10.1519/JSC.0000000000002582
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Abstract

Introduction

Low-intensity exercise combined with blood flow restriction (BFR) increases both muscle size and strength to a similar, or even greater extent than resistance training performed at higher intensities (1,4,31,33). This relatively new method of training involves the application of an inflatable cuff or tourniquet around the most proximal part of a limb to reduce arterial blood inflow to the working muscle and occlude venous return (30). Current research acknowledges the importance of prescribing an individualized cuff pressure (23,30) and further recommends setting a relative BFR pressure based on a percentage of the individual arterial occlusion pressure (AOP) (18,19,24). This approach is one of the most reliable and effective methods for cuff pressure prescription because it maximizes short- and long-term responses to low-intensity BFR exercise (18,19,24). Unfortunately, the direct quantification of AOP is often not available to all those exercising with BFR because it requires specific equipment, such as a portable Doppler unit. It was recently shown that arm circumference, as well as systolic and diastolic blood pressure (BP), all have great influence on upper-limb AOP (21). In fact, estimates of AOP can be calculated with reasonable success based on standardized regression models integrating these specific variables (12,16,21).

Despite the widespread use of low-intensity BFR training by both men and women (26), there is little information on the impact of BFR on women because of their underrepresentation in the literature (5). Further exploring this issue is highly relevant because there are several sexually dimorphic factors that likely influence the blood flow response to low-intensity BFR exercise. For instance, women have heightened muscle perfusion and capillarization than men as well as greater sensitivity to vascular changes in response to arterial occlusion (13,19,20). They also exhibit a higher relative proportion of appendicular fat and lower levels of lean mass (35). This is important because it reduces the transmission of external pressure to the vasculature and, therefore, the degree of BFR (11). However, the available literature has provided conflicting evidence regarding the influence of sex on AOP. Interestingly, although AOP follows a sexually dimorphic pattern in the standing position, this is not the case for supine measurements (16,21). Thus, there is compelling evidence that the hemodynamic challenge imposed by different body postures strongly determines the significance of the interaction between sex and AOP. Unfortunately, although most upper-limb exercise is completed in the seated position, it is not known whether the relationship of AOP with arm circumference and resting BP differs between men and women under these specific conditions. This may well be the case because the sitting posture influences resting hemodynamics (8). Considering all these aspects, we aimed at exploring whether the relationship of AOP with arm circumference and resting BP differs between men and women resting in the seated position. It was hypothesized that the indirect determination of seated AOP, based on arm circumference and systolic BP, would be improved by the addition of sex to the estimation model.

Methods

Experimental Approach to the Problem

This study involved one testing session designed to explore the relationship between AOP and its predictors in both men and women. Each testing session implicated taking direct resting measurements of AOP, arm circumference and BP in the seated position. All sessions were scheduled for the morning period to warrant similar conditions between participants and visits.

Subjects

We studied 62 young healthy participants on no medications (31 men: mean ± SD 21.7 ± 2.3 years; 31 women: 22.0 ± 2.0 years). All participants were active, accumulating 9 hours of physical activity per week as part of their academic work. Participation involved 1 testing session of ∼45 minutes. The risks implicated in the experimental design were carefully explained to each participant, and written informed consent was obtained before study entry. None of the women included in this study was pregnant or using oral contraceptives at the time of testing. In addition, they all had self-reported regular menstrual cycles of ∼28 days. The study complied with the principles set forth in the Declaration of Helsinki and was approved by the Faculty of Human Motricity's Ethics Committee (CEFMH Nº 4/2017).

Participants were all nonobese, normotensive (systolic and diastolic BP repeatedly ≤120/80 mm Hg (34)), nonsmokers, and free from any known cardiovascular, metabolic, respiratory, and orthopedic diseases as assessed by a health-screening questionnaire and baseline measurements. At study entry, each participant was required to complete a questionnaire for determining the degree of handedness (Waterloo Handedness Questionnaire–Revised; (7)). Testing was performed on the participants' dominant upper limb. Finally, participants were asked to maintain the same diet and to avoid physical exercise for at least 24 hours before testing.

Procedures

Tests were conducted during the morning period (between 8:00 and 12:00 hours) in a laboratory with an environmental temperature between 22 and 24° C and a relative humidity between 44 and 56%. On arrival at the laboratory, participants' body mass and height were taken to the nearest 0.01 kg (TANITA BF-350; Tanita Corporation of America, Inc., Arlington Heights, IL, USA) and 0.5 cm, respectively. Body mass index (BMI) was then calculated by dividing the participants' mass in kilograms by the square of their height in meters.

Testing involved the measurement of AOP, arm circumference, and BP in the seated position at resting conditions. The arm length of each participant was measured after taking the humerus of the dominant arm as an anatomical reference. The upper extremity of the humerus was located through palpation of the acromion process and marked with ink. Another ink mark was made at the lateral epicondyle of the humerus, with the arm at 90° of elbow flexion. Arm length was measured using a tape measure and was considered as the distance from the greater tuberculum of the humerus (tuberculum majus humeri) to the lateral epicondyle of the humerus (epicondylus lateralis humeri; (15)). Then, arm circumference was determined in each participant at 50% of their dominant arm length (arm relaxed and extended close to the trunk) (3).

Blood pressure was determined using an automatic BP monitor, in duplicate (Tango SunTech Medical, Morrisville, NC, USA), after 5 and 30 minutes of seated rest. For analysis, the average of the 2 resting BP values obtained at each time point was used. If the values were not within 5 mm Hg, a third measurement was taken and the 2 closest values were averaged and used for analysis. The measurements taken at time point #1 (after 5 minutes of seated rest) were used for exclusion of participants with abnormal resting BP (1 male participant). Those obtained at time point #2 (after 30 minutes of seated rest) allowed us to examine the stability of BP over time (before using it as a predictor of AOP). All measurements were performed with each participant seated comfortably, with back supported, legs uncrossed, and upper arm bare. As recommended by Pickering et al. (29), cuff size was selected based on the participants' arm circumference taken halfway between the acromion and olecranon processes. In addition, the participants' arm was supported at heart level. More specifically, the middle portion of the cuff was aligned with the right atrium, at the midpoint of the sternum.

All blood flow measurements were taken during seated rest, mimicking the position of the body during upper-limb exercise (e.g., seated biceps curl). Arterial blood flow was detected using a vascular Doppler probe (SONOLINE B LCD Fetal Doppler 8 MHz vascular probe; CONTEC Medical Systems CO., Ltd., China), placed over the radial artery, at the wrist level. Pulse was detected through auditory and visual signals obtained from the Doppler probe. A narrow 6 × 83 cm pneumatic cuff (SC5 Tourniquet Cuffs; D. E. Hokanson, Inc., Bellevue, WA, USA) was placed on the most proximal end of the dominant arm and inflated using a rapid inflation device (E20 Rapid Cuff Inflator; D. E. Hokanson, Inc.). The cuff was initially inflated to 50% of the individual resting systolic BP and then raised gradually up to the point when radial pulse was interrupted (9,16,18). Arterial occlusion pressure was recorded as the nearest 1 mm Hg pressure at which pulse was not present. Finally, as for BP, Doppler measurements were taken twice on the dominant arm to explore the stability of AOP over time (immediately after completing the first and second BP measurements). Arterial occlusion pressure taken at time point #2 was taken as the dependent variable.

Statistical Analyses

All data are reported as mean ± SD. Before comparing both groups of participants (men vs. women), data were tested for normality and homoscedasticity with the Kolmogorov-Smirnov and Levene's tests, respectively. The within-session stability of resting BP and AOP in each sex was explored using paired-sample t tests. Potential sex differences were evaluated using independent t tests. Multiple linear regression analysis was computed to determine whether sex, BP, and arm circumference (independent variables) were significant predictors of AOP (dependent variable). The interaction between sex and the other independent variables was also included in the models to explore sex differences in the association between BP, arm circumference, and AOP. Predictors were entered into the model in 2 blocks starting with block 1, which consisted of arm circumference and BP. The final block, block 2, added in sex and the interactions. Variables were then removed from the regression model whenever p > 0.05. Coefficient of determination (R2) was used to determine the percent of variance explained by each regression model. There was no concern regarding multicollinearity among predictor variables in multiple linear regression analysis (variance inflation factors <1.6).

A leave-one-participant-out approach was conducted to further validate the regression model for AOP prediction (32). Specifically, the model for each sex was run on the data from all participants in that group except one. Then, the resulting regression equation was used to predict the AOP of the previously excluded participant, obtaining the estimated AOP on a participant-by-participant basis. Paired t tests were used to explore the differences between actual and estimated AOP values within sexes. As a component of this method, we also determined the absolute percent error for the left-out participant, which was also calculated as:

Independent t tests were then used to evaluate the difference in absolute percent error between men and women. We also determined if absolute percent error, in each sex, differed significantly from zero. The agreement between actual and estimated AOP for the left-out participants was analyzed with Bland-Altman plots (Bland and Altman, 1999). Bland-Altman plots were analyzed for heteroscedasticity. This was performed by examining the R2 between the absolute difference and mean values (i.e., heteroscedasticity criteria set for R2 >0.1) (27).

Results

As shown in Table 1, both groups were of similar age and, despite being taller and heavier, men had similar BMI as women. Men also had higher systolic BP and larger arm circumference than women. Finally, there were no sex differences in diastolic BP or AOP. Figure 1 depicts BP and AOP values obtained in men and women at time points #1 and #2 (after 5 vs. 30 minutes of seated rest). Women exhibited a small, but significant decrease in systolic BP between time points. No other differences were noted for the remaining parameters included in Figure 1.

T1
Table 1.:
Characteristics of both groups of participants.*†
F1
Figure 1.:
Blood pressure and arterial occlusion pressure obtained in women (A) and men (B) at time points #1 and #2 (after 5 and 30 minutes of seated rest, respectively). SBP = systolic blood pressure; DBP = diastolic blood pressure; MAP = mean arterial pressure; AOP = arterial occlusion pressure. *p < 0.05, significant difference between time points.

Table 2 shows the hierarchical regression models for AOP prediction. We found that arm circumference, systolic BP, and sex were all significant predictors of seated AOP (p < 0.05). When compared with that seen in block 1, the inclusion of sex increased the proportion of variance in AOP (37 vs. 42%, respectively) explained by the model (F = 13.9; p < 0.001). For women, the prediction equation of AOP was: AOP (mm Hg) = 35.278 + (1.711 × arm circumference [cm]) + (0.47 × systolic BP [mm Hg]). For men, the prediction equation was: AOP (mm Hg) = 35.278 + (1.711 × arm circumference [cm]) + (0.47 × systolic BP [mm Hg]) − 5.704.

T2
Table 2.:
Univariate and multivariate models of linear regression for arterial occlusion pressure.*

The absolute percent error between actual and predicted AOP was similar in both sexes (men: −0.55 ± 7.12; women: −0.39 ± 6.31%, p > 0.05) and did not differ from zero in either men or women (p > 0.05). As depicted in Figure 2, the mean difference between actual and estimated AOP was on average nearly zero (men: −0.14; women: −0.01 mm Hg) and there was no systematic overestimation or underestimation. The agreement error had comparable 95% confidence intervals for both women and men (17.5 and 19.3 mm Hg, respectively), indicating similar predictability in individual AOP values between sexes. The R2 between the absolute difference and mean values was 0.113 and 0.405 for men and women, respectively. Therefore, the relationship between both variables was clearly heteroscedastic in women and approached homoscedasticity in men.

F2
Figure 2.:
Bland-Altman plots of the differences between actual and estimated arterial occlusion pressure (AOP) by the separate-group models as a function of mean AOP in women and men. The difference shown is that for each left-out participant in the cross-validation procedure. Solid and dashed lines represent mean difference and 95% limits of agreement, respectively.

Discussion

Our data indicate that seated AOP can be predicted from arm circumference, systolic BP, and sex. Specifically, we found that, when integrated in a regression model, these variables explain 42% of variance in AOP. This is in partial agreement with past research showing that arm circumference as well as systolic and diastolic BP explain most variance in AOP (16,21). We also established sex-specific regression equations for estimating individual AOP values for upper-limb BFR exercise performed in the seated position and this is relevant from a practical standpoint.

The results of the current study support the notion that arm circumference and systolic BP both influence AOP values. Arm circumference has great impact on the pressure required to restrict arterial blood flow. Its relevance for AOP estimation is even greater than that of limb composition (22). Thus, larger limb circumferences implicate higher levels of restrictive pressure to achieve the same level of BFR (22). This reinforces the need to assess the individual limb circumference before exercising with BFR. The effect of cuff width is also relevant, as it largely influences BFR pressure, with wider cuffs restricting blood flow at lower pressures than narrow cuffs (19,30). As recommended when performing upper-limb BFR exercise, we used a narrow cuff width (6 cm) in our experimental design (3,22,30). We then measured the absolute value of AOP (mm Hg) for each participant, determining it as the pressure where blood flow was interrupted to the point where auscultatory sounds could no longer be detected. Importantly, cuff inflation was performed to the nearest 1 mm Hg and this is different from that performed in past research (steep increments of 10 mm Hg) (21,22). The increased precision of AOP measurement is relevant to maximize the short- and long-term response to low-intensity BFR exercise (2,16,19,21).

The influence of brachial systolic BP on AOP is unequivocal because they both measure essentially the same physiological phenomenon (21). However, there is general agreement that the exclusive use of systolic BP for setting a given level of BFR may overestimate or underestimate the cuff pressure required for inducing significant neuromuscular adaptations (22). There is a poor relationship between systolic BP per se and percent values of AOP (12) and this indicates that BFR pressures should not be estimated exclusively from systolic BP. Interestingly, in women, we found that systolic BP decreased between 5 and 30 minutes of seated rest (∆ of ∼4 mm Hg). For this reason, the values of systolic BP taken after 5 minutes of rest were not used for the computing estimation model of AOP in either sex. Consequently, the use of this equation for AOP predictions based on measures of systolic BP obtained from women at an early stage of seated rest is not recommended (it might lead to an overestimation of AOP). As reported in past research, we found that mean arterial pressure is not predictive of upper-body BFR (2,12,21). As with mean arterial pressure, the inclusion of diastolic BP in the regression model did not add any value to the estimation of seated AOP. Interestingly, although some studies have shown diastolic BP to be a weak, but significant predictor of AOP measurements, this is not a universal finding (2,12,16,21). Such differences may arise from the overall impact of body position on resting hemodynamics (supine vs. sitting vs. standing position) (8). Thus, it may be concluded that although diastolic BP should be taken into consideration for AOP estimations in the supine and standing position, this is not the case for the seated position.

Because men and women exhibit physiological differences that likely trigger different responses to BFR, we also explored whether sex might add any predictive value to AOP estimation. Indeed, previous data have shown that women have enhanced muscle perfusion and capillarization (13) when compared with men. They also exhibit greater elevations in absolute and relative blood flow during exercise (28) and enhanced sensitivity to vascular changes (vasoconstriction and vasodilation) during acute occlusive events (20). As importantly, women demonstrate enhanced peripheral β-adrenergic–mediated forearm vasodilation (17). The vasodilatory response to acetylcholine, as well as peak reactive hyperemia also tends to be higher in women (28). Moreover, there is partial evidence that blood flow is more easily restricted in men because their larger muscle mass tends to exert more intramuscular pressure onto the feed arteries, thus limiting peripheral perfusion (14). This means that women require higher levels of absolute pressure (i.e., mm Hg) to achieve the same degree of BFR, thus corroborating our findings. Specifically, we found that, for a given value of brachial systolic BP and arm circumference, men attain complete vascular occlusion at lower restrictive pressures than women (β = −5.704).

Similarly to that seen in past reports (2,16,21), we also found that, followed by systolic BP (Std. β = 0.420), arm circumference explains most of AOP variance (Std. β = 0.439). However, we provide preliminary evidence that AOP prediction in the seated position is improved by the inclusion of sex (Std. β = −0.250) in the estimation model. Therefore, despite not interacting with arm circumference or systolic BP for AOP estimation, sex (per se) adds predictive power to the indirect determination of seated AOP. From a practical perspective, this is important because disregarding the role of sex for AOP prediction in persons of similar arm circumference and systolic BP would cause AOP overestimation and underestimation in men and women, respectively.

We also compared the estimated values of AOP with those of actual AOP obtained in each participant (using the leave-one-participant-out approach). According to our data, the error of AOP estimation displayed a heteroscedastic behavior in women (R2 between the absolute difference and mean values >0.1). Therefore, the error of estimation varies as a function of actual AOP (overestimation for greater AOP actual values and underestimation for lower AOP actual values) and this is more pronounced in women (women: R2 of 0.405 vs. men: R2 of 0.113). Nevertheless, our regression equation allows for a good estimation of upper-limb relative BFR pressure to use within the context of low-intensity BFR training. For example, based on our findings (Bland-Altman confidence levels of ∼17 and 19 mm Hg in women and men, respectively), when setting BFR to 60% of estimated AOP, the maximal deviation from 60% of actual AOP is −8 to +6% in women and −10 to +7% in men. These calculations were performed using the lower and upper limit of mean AOP values obtained for women and men (women: 118 and 168 mm Hg; men: 117 and 172 mm Hg). Although the upper-limit pressure (60 + 7% = 67% BFR) might bring no additional benefit for improving muscle strength and size (2,30), the lower limit (60 − 10% = 50% BFR) clearly falls within the margin of positive neuromuscular adaptations to this form of exercise training (40–60% AOP; (2)).

There are at least 3 important limitations to this study. First, despite having quantified the pressure required for arterial occlusion, we did not measure the change in blood flow. This is important because blood flow under relative levels of restriction has been shown to decrease in a nonlinear fashion (25). Nevertheless, determining the pressure of complete vascular occlusion allowed us to explore the role of sex in AOP estimation. Second, it has been previously shown that unilateral elbow flexion with low loads increases AOP by 31 mm Hg and that this decreases relative BFR pressure by ∼8% (2). Unfortunately, because we only measured AOP at resting conditions, we do not know whether sex differences in AOP estimation are sustained during exercise. This is important because such change in AOP values may influence chronic muscle adaptations in response to low-intensity blood flow–restricted exercise. Finally, we did not control for the effects of menstrual cycle on AOP. Past research has shown that BP changes during the menstrual cycle, reaching its highest values at the onset of menstruation (6). Moreover, there is compelling evidence that, in white women, the luteal phase is accompanied by α1-adrenergic vascular reactivity (10). For all these reasons, we cannot be certain that the predictive value of the equation derived for seated AOP estimation remains unchanged throughout the menstrual cycle.

Practical Applications

In conclusion, our data add novel information to the existent literature because the impact of sex on AOP prediction in the seated position had not been previously determined. Based on our findings, it is strongly recommended that seated AOP should be estimated based on individual arm circumference, systolic BP, and sex before performing upper-limb BFR exercise. The use of this approach, whenever direct measurements of AOP cannot be taken (e.g., Doppler unit not available), ensures a safer and more effective BFR exercise stimulus.

Acknowledgments

This work was supported by the Foundation for Science and Technology (FCT), Portugal (PTDC/DTP-DES/5714-2014).

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Keywords:

arterial occlusion pressure; resistance training; prediction

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