Comparison of Cardiac and Vascular Parameters in Powerlifters and Long-Distance Runners: Comparative Cross-Sectional Study

Background Cardiac remodeling is a specific response to exercise training and time exposure. We hypothesized that athletes engaging for long periods in high-intensity strength training show heart and/or vascular damage. Objective To compare cardiac characteristics (structure and function) and vascular function (flow-mediated dilation [FMD] and peripheral vascular resistance [PVR]) in powerlifters and long-distance runners. Methods We evaluated 40 high-performance athletes (powerlifters [PG], n = 16; runners [RG], n = 24) and assessed heart structure and function (echocardiography), systolic and diastolic blood pressure (SBP/DBP), FMD, PVR, maximum force (squat, bench press, and deadlift), and maximal oxygen uptake (spirometry). A Student’s t Test for independent samples and Pearson’s linear correlation were used (p < 0.05). Results PG showed higher SBP/DBP (p < 0.001); greater interventricular septum thickness (p < 0.001), posterior wall thickness (p < 0.001) and LV mass (p < 0.001). After adjusting LV mass by body surface area (BSA), no difference was observed. As for diastolic function, LV diastolic volume, wave E, wave e’, and E/e’ ratio were similar for both groups. However, LA volume (p = 0.016) and BSA-adjusted LA volume were lower in PG (p < 0.001). Systolic function (end-systolic volume and ejection fraction), and FMD were similar in both groups. However, higher PVR in PG was observed (p = 0.014). We found a correlation between the main cardiovascular changes and total weight lifted in PG. Conclusions Cardiovascular adaptations are dependent on training modality and the borderline structural cardiac changes are not accompanied by impaired function in powerlifters. However, a mild increase in blood pressure seems to be related to PVR rather than endothelial function.


Introduction
Exercise training induces cardiovascular adaptations secondary to changes in blood pressure as well as other hemodynamic and metabolic changes in response to physical exertion. These adaptive changes can induce left ventricular (LV) hypertrophy in the long run. 1 Some authors claim that borderline physiological and anatomical changes occur as part of an adaptive process of high-performance training and they have sparked off debate on their implications. 2 They postulate that volume overload generally increases LV pumping ability producing eccentric hypertrophy while, in contrast, pressure overload decreases ventricular cavity size producing concentric hypertrophy. Moreover, peripheral vascular resistance (PVR) is an important factor of cardiac overload by specifically modulating LV afterload. Furthermore, the endothelium is central to vasodilation by producing nitric oxide (NO), which is a vasodilator and has a direct effect on PVR. Therefore, it is important to highlight that after exercise there is a stimulation of NO production and eNOS phosphorylation, which contributes directly to a reduction in PVR. 3,4 Aerobic exercise increases shear stress leading to increased release and synthesis of NO and higher active muscle vasodilation. 5 LV pressure overload is reduced over time. 6 However, high-intensity resistance training such as weightlifting and powerlifting involves a number of very slow-speed contractions that produce transient mechanical compression of resistance vessels, increasing PVR and LV pressure overload during exercise. 7 It has been postulated that chronic increase in afterload induces the parallel addition of new sarcomeres in the myocardium leading to concentric ventricular hypertrophy. 8 Yet, this form of ventricular hypertrophy has not been demonstrated in strength training athletes, 9 and it is thus an inconsistent finding.
Given the limited body of evidence in support of these cardiovascular adaptations as well as concerning endothelial function and PVR in strength athletes, this study aimed to compare structural and functional cardiac changes in powerlifters and long-distance runners. Secondarily, we compared endothelium-dependent vasodilation and PVR in these athletes. Our hypothesis is that athletes engaging in high-intensity strength training for long periods of time show changes in cardiac structure associated with reduced cardiac function when compared to long-distance runners. Furthermore, long-time exposure to high-intensity strength training could lead to a reduction of endothelial function caused by pressure overload.

Study participant selection and groups
The study convenience sample comprised 40 male individuals aged 18-40 years. We selected athletes of powerlifting (powerlifters group [PG], n = 16) and long-distance (over 10 km) running events (runners group [RG], n = 24). Eligible athletes were those competing for at least 3 years. Individuals with any medical condition in the preceding 6 months; those not competing in the preceding 6 months; those on use of illicit (doping) substances in the last 12 months; or those who refused to sign an informed consent were excluded.
The study sample was recruited using an open invitation at training sites (gyms, health clubs and sports centers) and selected after applying the inclusion criteria. Participants were assessed as follows: on the first visit they underwent blood pressure assessment, echocardiographic assessment, brachial artery flow-mediated dilation (FMD), PVR assessments. In addition, they were administered a comprehensive questionnaire with questions about training including time of training experience; performance timeline; any awards/prizes; current training routine (volume, intensity, and duration of weekly training sessions, frequency of competitive participation, rest times, etc.) among others. On the next day, they underwent a maximum load test; and on the last visit (48 hours later), they underwent a maximum oxygen uptake test. All assessments were carried out within the same period of time (8 a.m. to 11 a.m.).

Blood pressure assessment
Blood pressure measurements were taken using a semi-automatic blood pressure monitor (OMROM 705CP), with the participant in a seated position with both feet on the floor, after a 10-minute rest; the cuff was placed and adjusted to the arm circumference. In a completely quiet room, blood pressure measurements were taken in duplicate on both arms, and the higher value of these readings was used in the study.

Echocardiographic examination
Transthoracic echocardiographic examinations were performed by an echocardiography specialist (G.B.G.). An ultrasound device (EnVisor CHD, Philips, Bothell, WA, USA) equipped with a sector transducer probe (2-4 MHz) was used to obtain longitudinal, cross-sectional, two-dimensional 2-and 4-chamber, and M module images. Continuous-wave, pulsed-wave, and color Doppler techniques were used to examine ventricular tissues and walls. All images were stored and sent to a second echocardiography specialist (D.P.K.) for blind evaluation of images. Body surface area (BSA) was calculated using Du Bois method. 10 Brachial artery flow-mediated dilation and peripheral vascular resistance We used a high-resolution two-dimensional Doppler ultrasound device (EnVisor CHD, Philips, Bothell, WA, USA) equipped with a high-frequency (7-12 MHz) linear vascular transducer probe and electrocardiographic imaging and monitoring software. FMD measurements were taken with the participants in the supine position, and a properly fitting pressure cuff was placed on the arm 5 cm above the cubital fossa. 11 Baseline brachial artery longitudinal diameters were assessed. Following that, the occlusion cuff was inflated to 50 mmHg above the systolic blood pressure (SBP) for 5 minutes and then deflated. Brachial artery diameters were measured for 60 seconds after deflation of the cuff. All analyses were performed offline and brachial artery measurements were made at the end of diastole (at R-wave peak on the electrocardiogram). FMD responses were expressed as percentage change from the baseline brachial artery diameter. PVR was calculated from mean blood pressure (MBP) and baseline blood flow obtained in the FMD test (PVR = MBP/ baseline blood flow in mmHg/cm.s -1 ).

Maximum load test
Maximum strength was assessed in the one-repetition maximum test (1-RM) for the squat, bench press and deadlift exercises, which are specifically performed at competitions, and through the total sum of these three exercises (total load). Distance runners attended a familiarization session within 48 hours of the test when the order of strength exercises and proper performance were introduced. For the 1-RM, the participants performed the maximum number of repetitions with the proposed load, up to a maximum of 10 repetitions. Exercise loads were increased according to Lombardi (1989) up to a point where participants were able to perform only one repetition with a maximum of 3 attempts to achieve the maximum load.

Maximum oxygen uptake
Maximum oxygen uptake (VO 2 peak or VO 2 max) was assessed through cardiopulmonary exercise test on a treadmill with respiratory gases collected (VO2000 model, Inbramed, Porto Alegre, Brazil). Powerlifters attended a familiarization session within 48 hours of the test where test procedures were introduced (Bruce protocol and mask placement for gas collection). The highest value, either VO 2 peak or VO 2 max was recorded at the end of the test as VO 2 max.

Statistical analyses
We performed the Shapiro-Wilk test to test normality of the data and homogeneity of variance was tested using Levene's test. All results are described as mean ± SD and confidence interval. We conducted Student's t Test for independent samples to assess differences between groups and calculated Pearson's linear correlation coefficients (α = 0.05 for all tests). All statistical analyses were performed using SPSS Statistics (version 21 for Windows).

Results
The participants had similar age and height (Table 1). However, all anthropometric measurements for PG were greater compared to distance RG. In turn, Table 2 shows loads for the squat, bench press, and deadlift exercises and total load (total sum of these three exercises). For all types of exercises, weight loads were higher in PG than RG as expected. The total load was greater by ~133% in PG than RG. The differences remained unchanged when loads were adjusted for body mass. Table 3 shows hemodynamic and cardiopulmonary parameters. Powerlifters had higher resting SBP (~10%) and resting DBP (~12%); the absolute differences between the two groups were 13.6 mmHg and 10.1 mmHg, respectively. Resting heart rate was higher in PG compared to RG (~19%, Δ15.7 bpm). VO 2 max was much higher in RG than PG (~65%): the highest VO 2 max value among powerlifters was lower than the lowest VO 2 max value among runners. Table 4 shows the echocardiographic results. As for cardiovascular adaptations, aorta diameter, left atrium (LA) diameter, right ventricle diameter, LV systolic diameter, and LV diastolic diameter were similar in both groups. However, PG showed greater interventricular septum thickness (Δ2.4 mm) and posterior wall thickness (Δ1.2 mm). They also showed greater LV mass (Δ46.5 g), but this difference disappeared after adjusting for BSA. As for diastolic function, LV diastolic volume, transmitral E wave, e' wave, and E/e' ratio were similar in both groups. However, LA volume (~22%), and LA volume adjusted for BSA (~40%) were found in PG, when compared to RG, but they were all within normal ranges. Although PG showed some degree of anatomical remodeling and different diastolic function parameters compared to RG, systolic function reflected in LV systolic volume, ejection fraction, and ejection fraction calculated by Simpson's rule were similar in both groups. Of the 40 participants, 9 (22.5%) had physiological ventricular hypertrophy in response to exercise; 10 (all powerlifters) had interventricular septum thickness greater than 11 mm. Of the 27 participants with LV mass greater than 225 g and LV mass adjusted by BSA greater than 115g/m 2 , 13 (82%) were PG and 14 (63%) RG. The correlations between training parameters and echocardiographic and cardiopulmonary variables in PG are displayed in Table 5. There was a direct correlation between interventricular septum thickness and weight load in the deadlift, squat, and total load. Interestingly, no correlation was found with time of exposure, i.e., duration in years of strength training among powerlifters. SBP levels were directly correlated with training intensity; and DBP showed a stronger correlation with duration of strength training. For runners, interventricular septum thickness and resting heart rate were inversely correlated with VO 2 max and duration of strength training (Table 6).
Finally, FMD measurements were directly proportional to training intensity (% 1-RM) in PG and weight load for the squat (Table 7). For RG, no correlation of FMD values was found with cardiopulmonary variables and resting heart rate. Furthermore, FMD values were correlated with duration of powerlifting training (years) and daily duration of training session. However, this same correlation was not seen among runners. 12

Discussion
Our study found that, compared with long-distance runners, powerlifters showed greater interventricular septum thickness, LV posterior wall thickness and LV mass. However, after adjusting for BSA, no difference was observed in LV mass.Cardiac function was similar in powerlifters and runners. Together, these parameters suggest that specific cardiac remodeling may occur as a result of training, but with no impairment of cardiac functions. A major finding of our study was similar FMD measurements in both powerlifters and runners despite PVR being higher in powerlifters. 12 Although our findings are comparative and derive from a cross-sectional design, they suggest that high-intensity strength training does not necessarily cause damaging cardiovascular changes as it has been generally believed.

Cardiac parameters
Regarding cardiac parameters (anatomical structure, and diastolic and systolic function), the echocardiographic assessments showed increased interventricular septum thickness with slight or no chamber diameter reduction and slight increase in posterior wall thickness in powerlifters compared to runners. These changes may be because powerlifting involves a great amount of slow-speed contractions using high loads close to the maximum 13 in daily training sessions leading to LV pressure overload. As for the cutoff values, several studies with high-performance athletes have used to determine pathological hypertrophy cutoff values of 12-13 mm for maximum interventricular septum thickness and 55-60 mm for end-diastolic dimension, as described below.Whyte (2004) examined 306British elite male athletes (judo, n = 22; skiing, n = 10; pole vault, n = 10; kayak, n = 11; rowing, n = 17; cycling, n = 11; power lifters, n = 29; triathlon, n = 51; modern pentathlon, n = 22; middle distance, n = 45; rugby, n=30; tennis, n = 33; swimming, n = 19) and found interventricular septum thickness > 13 mm in ~3.0% of them. Riding (2012) examined 836 athletes (soccer, n = 586; basketball, n = 75; volleyball, n = 41 and handball, n = 35) and found interventricular septum thickness > 12 mm and typical features of concentric left  wrestling, n = 14; judo, n = 13; luge, n = 13; field hockey, n = 13; table tennis, n=11; pentathlon, n = 7; weight-lifting, n = 7; golfing, n = 6; baseball, n=5; triathlon, n = 3; motor-racing, n = 3; body-building, n=3; other modalities n = 72) and found interventricular septum thickness > 13 mm in 1.1% of them. Moreover, they also found that 45% and 14% of the athletes studied exhibited end-diastolic dimension > 55 mm and > 60 mm, respectively. Thus, if we use these cutoffs, despite some anatomical cardiac changes, none of the study participants showed cardiac dimensions consistent with pathological hypertrophy. However, it is important to note a strong correlation between weight loads lifted in the squat and total load and cardiac dimensions including septum thickness, posterior wall thickness, and LV mass. Yet again, a possible explanation is that powerlifting involves a great amount of slow-speed contractions using high loads close to the maximum leading to a pressure overload. [9][10][11][12][13][14][15][16][17] With regard to LV mass, Gardin et al., 18 reported values of 225 g and 115 g/m² adjusted by BSA in individuals chronically exposed to pressure overload. LV mass was also measured in our study and we found values of 282 g and 135 g/m 2, among powerlifters. Interestingly, runners also showed high LV mass (236 g and 128 g/m 2 adjusted by BSA). Regardless of the training modality, cardiac remodeling occurred in response to exercise training in both groups. Though still controversial, echocardiographic measurements indexed to BSA allow to   comparing individuals of different body sizes. BSA is affected by fat mass, and fat mass is neither correlated with nor predicts LV mass. 19 An alternative approach is to adjust echocardiographic parameters for lean mass. However, accurate measurements are not widely available and substitute methods such as skin-fold thickness measurements are relatively inaccurate. 20,21 Diastolic function assessment in the study revealed consistently normal values in long-distance runners. 22 In contrast, lower LA volume and transmitral A-wave velocity measures were found in powerlifters although these values were within normal limits. The difference of LA volume measures between both groups was ~22%, and it was even more pronounced after adjustment for BSA (~40%). D'Andrea et al., 23 and coworkers have assessed LA volume and BSA-indexed LA volume in 350 endurance athletes and 245 strength athletes. 23 For BSA-indexed measures, these authors defined values between 29 and 33 mL/m 2 as mild LA enlargement and values greater than 33 mL/m 2 as moderate LA enlargement. Thus, our results were all below the cutoff values set in D'Andrea et al., 23 As for LV systolic function assessed through estimates of ejection fraction and ejection fraction calculated by Simpson's rule, the echocardiographic assessment showed values within the normal range in all cases.

Blood pressure
The association of aerobic training with lower resting blood pressure is well established. 24,25 But a growing body of evidence shows that strength training can have a similar effect on blood pressure, 26 though there is not yet a consensus in the literature. 27 However, high-intensity strength training has been reported to negatively affect blood pressure.
A meta-analysis showed that training modalities that basically consist of strength training (powerlifting, bodybuilding, and Olympic weightlifting) are associated with a higher risk of high blood pressure with mean SBP of 131.3 ± 5.3 mmHg and mean DBP of 77.3 ± 1.4 mmHg. 28 These values are consistent with those found in our study (SBP 130.0 ± 8.2 and DBP 82.1 ± 6.9 mmHg).

Vascular function
FMD measurements were similar in both powerlifters and runners. This is an interesting finding given that these two training modalities have different biomechanical and metabolic characteristics. Exercise training has been shown as an effective means for the improvement of endotheliumdependent vasodilation capacity. 29 Among high-performance athletes, long-distance runners with above average normal cardiac function show lower arterial stiffness, lower oxidative stress, and increased endothelium-dependent dilation 30 capacity when compared to sedentary individuals of the same age. 31 These data suggest that outstanding cardiac performance in athletes may be associated with improved vascular function induced by aerobic exercise training.
It is well known that aerobic exercise improves endothelial function by producing increased shear stress on the vessel walls during exercise. 32 Yet, it has been suggested that strength training can increase hemodynamic stress due to the mechanical compression of blood vessels during active movements together with excessive vascular tension produced during strength exercises. 7 Thus, we can speculate that high-intensity strength training could acutely affect endothelium-dependent vasodilation and lead to permanent damage in the long run. In this regard, impaired vascular function has been demonstrated in strength athletes, though it appears to be related to the use of anabolic agents rather than an effect of training. 33,34 Heffernan et al. found increased forearm reactive hyperemia in healthy young individuals after 6-month strength training. 35 The most likely explanation for increased endothelium-dependent dilation in strength training is the assumption of the mechanical compression of resistance vessel walls during exercise, followed by blood flow release after cessation of exercise, producing a sharp increase in vessel wall shear stress. 36 Although training modalities involve different stimuli (running training: increased continuous blood flow; strength training: intermittent compression of the muscles and restoring blood flow) they ultimately produce the same effects on vessel wall shear stress.
It is important to note that, despite increased blood pressure levels and greater posterior wall thickness and LV mass found in our study among powerlifters, they showed no cardiac and endothelial function impairment when compared to runners and all the parameters were above average. Therefore, high blood pressure found in powerlifters seems to be related to increased PVR rather than endothelial function impairment.

Study strengths and limitations
The key strengths of our study are the use of a homogeneous sample (within each group) and that all echocardiographic images were assessed by two independent examiners, one of them blinded. However, our data should be interpreted with caution due to some limitations including the small sample size (due to recruitment challenges as anabolic steroid use is common among powerlifters and few met our inclusion criteria), and the challenge of recruiting a sample of untrained healthy subjects; however, all parameters evaluated were compared with those findings of other studies and/or current guidelines.

Conclusion
Our study showed that cardiac remodeling seems dependent on training modalities and not on structural difference, as in BSA-indexed LV mass in both powerlifters and long-distance runners. Systolic and diastolic functions were preserved in both modalities. Powerlifters showed higher resting blood pressure, which can be explained by increased PVR. However, FMD measurements were similar in both groups studied and were well above average. Although our findings are comparative in nature and derive from a cross-sectional design, it is possible to speculate that high-intensity strength training for a significant number of years (~5 years or more) may be associated to borderline structural cardiac changes, though they are not accompanied by reduced cardiac function.

Author contributions
Conception and design of the research: Silva DV, Lehnen AM; Acquisition of data, Analysis and interpretation of the data, Statistical analysis and Writing of the manuscript: Silva DV, Waclawovsky G, Kramer AB, Stein C, Eibel B, Grezzana GB, Schaun MI, Lehnen AM; Obtaining financing: Waclawovsky G, Lehnen AM; Critical revision of the manuscript for intellectual content: Waclawovsky G, Eibel B, Grezzana GB, Schaun MI, Lehnen AM.

Potential Conflict of Interest
No potential conflict of interest relevant to this article was reported.

Sources of Funding
There were no external funding sources for this study.

Study Association
This article is part of the thesis of master submitted Diego Vidaletti Silva, from Instituto de Cardiologia -Fundação Universitária de Cardiologia (IC/FUC).

Ethics approval and consent to participate
This study was approved by the Ethics Committee of the Instituto de Cardiologia do RS / Fundação Universitária de Cardiologia under the protocol number #417492. All the procedures in this study were in accordance with the 1975 Helsinki Declaration, updated in 2013. Informed consent was obtained from all participants included in the study.