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356 Clinical Sciences

Associations of Maximal Strength and Muscular


Endurance with Cardiovascular Risk Factors

Authors J. P. Vaara1,5, M. Fogelholm2, T. Vasankari3, M. Santtila4, K. Häkkinen5, H. Kyröläinen1,5

Affiliations Affiliation addresses are listed at the end of the article

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Key words Abstract tory fitness. Muscular endurance was negatively

▶ muscular fitness
▼ associated with the clustered cardiovascular risk

▶ cardiorespiratory fitness
The aim was to study the associations of maximal factor independent of cardiorespiratory fitness

▶ cardiometabolic risk factors
strength and muscular endurance with single and (β = − 0.26, p < 0.05), whereas maximal strength

▶ waist circumference
clustered cardiovascular risk factors. Muscular was not associated with any of the cardiovas-
endurance, maximal strength, cardiorespiratory cular risk factors or the clustered cardiovascular
fitness and waist circumference were measured risk factor independent of cardiorespiratory fit-
in 686 young men (25 ± 5 years). Cardiovascular ness. Furthermore, cardiorespiratory fitness was
risk factors (plasma glucose, serum high- and inversely associated with triglycerides, s-LDL-
low-density lipoprotein cholesterol, triglycer- cholesterol and the clustered cardiovascular
ides, blood pressure) were determined. The risk risk factor (β = − 0.14 to − 0.24, p < 0.005), as well
factors were transformed to z-scores and the as positively with s-HDL cholesterol (β = 0.11,
mean of values formed clustered cardiovascular p < 0.05) independent of muscular fitness. This
risk factor. Muscular endurance was inversely cross-sectional study demonstrated that in
associated with triglycerides, s-LDL-cholesterol, young men muscular endurance and cardiores-
glucose and blood pressure (β = − 0.09 to − 0.23, piratory fitness were independently associated
p < 0.05), and positively with s-HDL cholesterol with the clustering of cardiovascular risk factors,
(β = 0.17, p < 0.001) independent of cardiorespira- whereas maximal strength was not.

Introduction [5, 19, 20]. Nevertheless, some studies have


accepted after revision
May 24, 2013
▼ shown attenuated or non-significant association
Adolescents and young adults are generally at a between muscular fitness and CVD risk factors
low risk for having cardiovascular diseases. How- after adjustment for cardiorespiratory fitness
Bibliography
DOI http://dx.doi.org/ ever, the risk factors may develop and especially, [20, 32], whereas some studies have shown sig-
10.1055/s-0033-1349092 track into later life in adulthood [6, 26]. The com- nificant associations independent of cardiorespi-
Published online: mon risk factors for cardiovascular diseases ratory fitness [3, 13, 30, 32]. As a consequence,
November 10, 2013 (CVD) include blood pressure, impaired glucose the information available of the independent
Int J Sports Med 2014; 35: metabolism, elevated concentration of triglycer- association of muscular fitness and CVD risk fac-
356–360 © Georg Thieme
ides and low level of high-density lipoprotein tors is still scarce.
Verlag KG Stuttgart · New York
cholesterol [10, 29]. Previous studies have shown The risk for cardiovascular disease increases as
ISSN 0172-4622
that cardiorespiratory fitness (CRF) and body the number of risk factors increases [8]. There-
Correspondence composition are related to cardiovascular risk fore, the presence of multiple risk factors has
Jani P. Vaara factors [11, 12, 25, 27, 29]. Although some studies been used to estimate increased risk for cardio-
The Department of Leadership have assessed the relationship between the CVD vascular diseases in previous studies [2, 12, 24].
and Military Pedagogy risk factors and muscular fitness over the recent The present study used both single and clustered
National Defence University years, the evidence of its influence on the risk cardiovascular risk factors of plasma glucose
Santahamina
factors independent of cardiorespiratory fitness (GLUC) concentration and serum high-density
00860 Helsinki
Finland
remains less clear [4]. lipoprotein cholesterol (HDL), low-density lipo-
Tel.: + 358/299/530 432 Inverse associations with muscular fitness and protein cholesterol (LDL), triglycerides (TG) as
Fax: + 358/299/530 431 prevalence of metabolic syndrome have previ- well as blood pressure (BP) as the main outcome
jani.vaara@mil.fi ously been reported in cross sectional studies (dependent) variable. We hypothesized that

Vaara JP et al. Associations of Maximal Strength … Int J Sports Med 2014; 35: 356–360
Clinical Sciences 357

maximal strength and muscular endurance are associated with fast, and were centrifuged at speed of 3 500 rpm. Plasma glucose
single and the clustered cardiovascular risk factors independent (GLUC) and serum high density lipoprotein (HDL) and triglycer-
of cardiorespiratory fitness. The main question to be answered ides (TG) were analyzed by Konelab 20 XTi -device (Thermo Elec-
was whether muscular or cardiorespiratory fitness is more tron Co, Vantaa, Finland), and the isolated LDL fraction was used
strongly related to the clustered cardiovascular risk factor score for direct measurement of LDL-cholesterol (CHOD-PAP method).
independent of one another. To the best of our knowledge, this is The ranges for CHOL, TG, HDL and LDL assays varied from 0.1–15;
the first study using both muscular endurance and maximal 0.09–11; 0.04–2.84 and 0.3–8.9 mmol.l − 1, respectively. Intra- and
strength to assess the association of muscular fitness with single inter-assay coefficients of variance were 1.1 % and 2.1 % for CHOL,
and clustered risk factor for cardiovascular diseases. 1.0 % and 3.8 % for TG, 3.4 and 3.9 for LDL, and 0.5 %, 7.6 % for HDL,
respectively. Sensitivity for GLUC was 0.1 mmol/l, and intra- and
inter-assay coefficients of variance were 1.0 and 2.0 %, respec-
Methods tively. A continuous cardiovascular risk factor score was used in
▼ the present study similar to earlier studies [30, 31]. First, the val-
Participants ues of each cardiovascular risk factor (plasma glucose, serum trig-
Participants were 846 young (25.5 ± 5.0 years) adult Finnish lycerides, serum high-density lipoprotein cholesterol, serum

This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
men, who were called up to military refresher training organ- low-density lipoprotein cholesterol, systolic and diastolic blood
ized by the Finnish Defence Forces. Only those volunteers who pressure) were transformed to z-scores. HDL cholesterol was
completed all of the physical fitness tests, waist circumference inverted before being included in the risk score. The continuous
and blood pressure measurements as well as the blood sample clustered cardiovascular risk factor score was calculated from the
draws were included in the data analysis. As a result, the final mean of z-score values of all cardiovascular risk factors.
study sample consisted of 686 healthy young adult men free of
cardiovascular or other diseases. The present study sample was Muscular endurance and maximal strength tests: Tests for
compared to corresponding cohorts of 20–30-year old Finnish muscular endurance consisted of push-ups, sit-ups and repeated
men in the national register data (Statistics Finland) from the squats. The duration of each test was 60 s. There was a recovery
years of 2007–2008 for age, education and place of residence. period of 5 min between the tests. Participants were instructed
The present study sample is not fully representative of the in correct technique before each test. Only the completed trials
nation, since the northern part of Finland was underrepresented with adequate technique were accepted for final results. Maxi-
in this study sample and those with 13–15 years of education mal isometric force of leg extension and bench press (both
were overrepresented. All participants provided written regarded as tests for maximal strength) were measured using a
informed consent. The study was conducted according to the dynamometer. Knee angle was set to 107 ° with a goniometer,
ethical standards of the International Journal of Sports Medi- and hands were set on handle grip in the leg extension test [17].
cine, described by [15] and was approved by the ethical commit- During the maximal bench press test, the participants were in a
tee of the Central Finland Health Care District and the supine position with their back flat on a bench and feet flat on
Headquarters of the Finnish Defence Forces. the floor with elbow and shoulder joints positioned at 90 °. A
warm-up series of at least 2 submaximal sets was performed
Study procedures prior to maximal sets. 3 trials were performed using a 30 s recov-
Call up to military refresher training and information on the ery period. The best performance was included in the analysis.
study plan were sent 5 months before measurements. The meas- Each participant was advised to produce maximal force as fast as
urements were carried out in 8 different sessions during the possible and to maintain it for 3 s. The participants were verbally
year 2008. Participants reported to bases by 2:00 p.m. The study encouraged during the maximal efforts by the test personnel.
protocol was explained in detail to the participants before they Maximal force was recorded with AD-converter (CED power
gave their written consent. They also completed a questionnaire 1401, Cambridge Electronic Design, ltd., England) at the fre-
gathering background information (e. g. age, smoking), health quency of 1-kHz on a computer. Data was analyzed with Signal
behaviour (e. g. leisure time physical activity, LTPA) and contain- (2.16) software. The results of maximal strength and muscular
ing questions for screening possible health contraindications for endurance were further expressed as the test score per kilogram
physical fitness tests. The participants were divided into groups of body weight similar to previous studies [19, 20, 30]. The
of 10 persons for the measurements, which started on the next results of the muscular endurance and maximal isometric
morning at 5:50 a.m. after a night of sleep with an overnight fast. strength test scores were then transformed to z-scores. The
Blood pressure and body composition were measured, and blood mean of z-scores of each muscular endurance test formed a
samples were drawn. The participants then ate a light breakfast muscular endurance index (MEI), and the mean of maximal
and drank a maximum of one cup of coffee or tea before under- strength tests formed a maximal strength index (MSI).
going measurements of bilateral maximal isometric force of leg
and arm extensors. Finally, an indirect graded cycle ergometer Cardiorespiratory fitness: Maximal aerobic capacity (VO2max)
test until exhaustion and tests of muscular endurance (push- was determined using an indirect graded cycle ergometer test
ups, sit-ups, repeated squats) were performed. (Ergoline 800 S, Ergoselect 100 K, Ergoselect 200 K, Bitz, Ger-
many). A progressive protocol was used, which initially started
Selected cardiovascular risk factors: Blood pressure was at power output of 50 W and was increased 25 W every 2 min
recorded twice at 1–2 min intervals in a seated position using an until exhaustion (volitional will to finish or a decrease of pedal-
automatic blood pressure device (Omron M6 Comfort, Nether- ling cadence under 60 rpm/min). Heart rate (HR) was recorded
lands). In the analysis, a mean of the 2 values were used. Blood continuously during the test using heart rate monitors (Polar
samples were drawn from the antecubital vein using Terumon Vantage NV or S610, S710 or S810, Kempele, Finland). Predicted
Venosafe (Terumo Europe, Leuven, Belgium) after an overnight VO2max was determined from HR and maximal power (Watts,

Vaara JP et al. Associations of Maximal Strength … Int J Sports Med 2014; 35: 356–360
358 Clinical Sciences

W) (Fitware, Mikkeli, Finland) with the following equation: least 4 times a week. LTPA was classified as low (responses 1–2),
VO2max (ml · kg − 1 · min − 1) = 12.35*Pmax/kg + 3.5, where Pmax is moderate (responses 3–4) and high (responses 5–6) activity.
maximal power and kg body mass in kilograms. The intra-class
correlation among men has been reported to be high with this Statistical analysis
method (ICC r = 0.82–0.94) [28]. The participants who reported using medication for diabetes,
Waist circumference was measured twice with a tape measurer high cholesterol or hypertension (n = 8) were excluded of the sta-
at the level of iliac crest after exhaling. tistical analysis. The final study sample consisted of 686 partici-
Self-reported leisure-time physical activity (LTPA) was ascer- pants. Data were analyzed with PASW-software (PASW for
tained using the following question: “In which of the following Windows 18.0.1). Descriptive statistics as means and SD and
leisure time physical activity group are you engaged? – (“Think were calculated for the study sample. Multinomial logistic
about the last 3 months and consider all leisure time physical regression was used to study the associations of cardiorespira-
activity that had lasted at least 20 min per session”). Response tory and muscular fitness with single and the clustered cardio-
categories were: (1) less than once a week, (2) no vigorous activ- vascular risk factors using models with different combinations
ities, but light or moderate physical activity at least once a week of covariates (smoking, age, fitness variables, waist circumfer-
(3) vigorous activity once a week (4) vigorous activity twice a ence and self-reported leisure time physical activity).

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week (5) vigorous activity 3 times a week (6) vigorous activity at

Results

Table 1 Characteristics of the study sample (n = 686). The descriptive data on body composition, physical fitness tests
and cardiovascular risk factors are shown in ● ▶ Table 1.
mean s.d.
Maximal strength was inversely associated with triglycerides,
age (year) 25.0 4.6
LDL-cholesterol, systolic and diastolic blood pressure after
height (cm) 180.1 6.3
adjustment for age and smoking. However, after adjustment for
body mass (kg) 80.6 13.4
waist (cm) 86.3 10.4
cardiorespiratory fitness, a positive association was found only
body mass index 24.8 3.8 between maximal strength and diastolic blood pressure. Muscu-
repeated squats (reps/min) 43.7 8.5 lar endurance was associated with all of the cardiovascular risk
sit-ups (reps/min) 38.0 10.2 factors, while the further adjustment for cardiorespiratory fit-
push-ups (reps/min) 28.8 12.8 ness attenuated these associations. However, each remained sta-
leg extension force (N) 2 943 873 tistically significant (●
▶ Table 2).

bench press force (N) 900 199 Cardiorespiratory fitness was inversely associated with all of the
VO2max (mL · min-1 · k-1) 41.6 8.1 cardiovascular risk factors except for HDL-cholesterol after
maximal heart rate (beats/min) 192 8
adjustment for age and smoking. While attenuated by the fur-
maximal load (W) 244 46
ther adjustment for maximal strength and muscular fitness,
cholesterol (mmol/L) 4.53 0.86
associations with LDL-cholesterol, HDL-cholesterol and triglyc-
HDL (mmol/L) 1.49 0.36
LDL (mmol/L) 2.43 0.63
erides remain statistically significant (●
▶ Table 2).

triglycerides (mmol/L) 1.03 0.53 Maximal strength, muscular endurance and cardiorespiratory
glucose (mmol/L) 5.40 0.41 fitness were all inversely associated with the continuous clus-
systolic blood pressure (mmHg) 123.0 11.8 tered cardiovascular risk factor score following adjustment for
diastolic blood pressure (mmHg) 76.8 8.4 age and smoking. In addition, muscular endurance was inversely
distribution of leisure-time physical activity: associated with the clustered risk factor independent of cardi-
low group 31.2 % orespiratory fitness, whereas maximal strength was not inde-
moderate group 38.7 % pendently associated. Cardiorespiratory fitness was inversely
high group 30.1 % associated with the clustered risk factor independent of maxi-

Table 2 The associations of maximal strength, muscular endurance and cardiorespiratory fitness with single cardiovascular risk factors (the standardized
β-coefficients from multivariate regression models).

s-LDL s-HDL Serum- Plasma Systolic blood Diastolic blood


cholesterol cholesterol triglycerides glucose pressure pressure
maximal strength index (MSI)
model A − 0.12 *** 0.07 − 0.12 *** − 0.04 − 0.07 * − 0.14 ***
model B ‡ − 0.05 0.003 − 0.02 0.0001 − 0.04 0.08 *
muscular endurance index (MEI)
model A − 0.23 *** 0.24 *** − 0.25 *** − 0.16 *** − 0.22 *** − 0.21 ***
model B ‡ − 0.15 ** 0.17 *** − 0.09 * − 0.14 ** − 0.23 *** − 0.17 ***
cardiorespiratory fitness (CRF)
model A − 0.22 *** 0.21 *** − 0.30 *** − 0.13 *** − 0.11 ** − 0.17 ***
model B † − 0.14 ** 0.11 * − 0.24 *** − 0.02 0.03 − 0.08
Model A adjusted for age and smoking
‡ Model B adjusted for age, smoking and CRF
† Model B adjusted for age, smoking, MSI and MEI
***p < 0.001, ** p < 0.005, *p < 0.05

Vaara JP et al. Associations of Maximal Strength … Int J Sports Med 2014; 35: 356–360
Clinical Sciences 359

muscular fitness scores have been used [21, 22, 30], whereas in
Table 3 Associations of maximal strength, muscular endurance and cardio-
respiratory fitness with continuous clustered cardiovascular risk factor score others the muscular fitness score has been divided by body mass
(the standardized β-coefficients from multivariate regression models). [3, 19, 20, 30] or fat-free mass [5, 32]. The findings from the
present study suggest that future studies are warranted to
Maximal Muscular Cardiorespira- clearly distinguish between muscular endurance and maximal
strength endurance tory fitness strength due to their different associations to cardiovascular risk
model A − 0.16 *** − 0.37 *** − 0.32 *** factors, body composition and other fitness parameters [31].
model B 0.06 ‡ − 0.26 * ‡ − 0.16 *** † Maximal strength was, however, associated positively with
model C 0.04 ‡ − 0.05 ‡ − 0.08 † diastolic blood pressure. Similarly in a previous cross-sectional
Model A adjusted for age and smoking study, an adverse association has been found between maximal
‡ Model B adjusted for age, smoking and CRF
strength and high-density lipoprotein cholesterol as well as trig-
† Model B adjusted for age, smoking, MSI and MEI
lycerides after being controlled for age, cardiorespiratory fitness
‡ Model C adjusted for age, smoking, waist circumference and CRF
† Model C adjusted for age, smoking, waist circumference, MSI and MEI and sum of skinfolds [22]. In addition, some cross-sectional
***p < 0.001, ** p < 0.005, *p < 0.05 studies have also reported adverse relationships between physi-
cal activity and blood pressure [7, 16]. The biological mecha-
mal strength and muscular endurance (●

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▶ Table 3). In addition, nisms for these remain unknown. However, some confounders
when waist circumference was further adjusted in the regres- may play a role as mediators, such as nutritional factors (salt
sion models, the associations of cardiorespiratory fitness and intake) or stress, none of which were studied in the previous or
muscular endurance with single and the clustered CVD risk fac- the present study. It is, however, of noteworthy that maximal
tors became non-significant. Moreover, in a model that includes strength has other health benefits, especially for older individu-
waist circumference and all fitness parameters, the strongest als, including prevention of sarcopenia and maintenance of
relationship was observed between waist circumference and the mobility.
clustered CVD risk factor score (β = 0.41, p < 0.001), leaving all fit- Cardiorespiratory fitness was associated with the clustered CVD
ness parameters non-significant. Additional adjustment for lei- risk factor independent of muscular fitness in line with previous
sure time physical activity did not have a significant effect on studies [11, 12, 25, 27, 32]. The present study revealed similar
the associations between maximal strength, muscular endur- relationships in single cardiovascular risk factors except for glu-
ance, cardiorespiratory fitness and the single or clustered cardi- cose and blood pressure.
ovascular risk factor score. The present study observed a stronger association between
waist circumference and the clustered cardiovascular risk factor
compared to cardiorespiratory fitness and muscular endurance,
Discussion which is in line with most of the cross-sectional studies
▼ [9, 18, 23, 25]. Nevertheless, rather similar magnitudes of cardi-
The main findings of the present cross-sectional study of young orespiratory fitness and waist circumference as predictors of
adult men demonstrate that muscular endurance was inversely CVD risk factors have also been observed [12]. The physiological
associated with the clustered cardiovascular risk factor score mechanisms behind the potential cardioprotective effect of car-
independent of cardiorespiratory fitness, whereas maximal diorespiratory fitness include reduced concentrations of inflam-
strength was not associated therewith. Secondly, cardiorespira- matory markers and oxidized LDL lipids, improved endothelial
tory fitness was inversely associated with the clustered cardio- function, lipoprotein subclass distribution and postprandial
vascular risk factor score independent of muscular fitness, and lipoprotein metabolism [1, 14].
the strongest association was found between waist circumfer-
ence and the clustered cardiovascular risk factor score inde- Strength and limitations
pendent of muscular and cardiorespiratory fitness. The strength of the present study is the extensive data set
Muscular endurance was inversely associated with blood pres- including physical fitness of cardiorespiratory and the dimen-
sure, glucose, triglycerides, LDL-cholesterol and the clustered sions of muscular fitness. The detailed measurements of muscu-
cardiovascular risk factor, and positively associated with HDL- lar fitness (muscular endurance, maximal strength) are rare in
cholesterol independent of cardiorespiratory fitness. On the the previous studies. Nevertheless, there are some limitations
other hand, maximal strength was not associated with any of the that have to be considered. Predicted VO2max was used instead
single or the clustered cardiovascular risk factor independent of of a direct measurement in the present study. Moreover, we
cardiorespiratory fitness in the present study. Earlier cross-sec- were not able to take into account some possible confounding
tional studies have shown an inverse association between car- factors, such as nutrition and stress. Finally, due to the cross-
diovascular risk factors and muscular fitness index [3, 13, 21, 30] sectional study design, the causality of the relationships cannot
and maximal strength [5, 19, 20, 32]. After adjustment for cardi- be assessed.
orespiratory fitness, these associations have, however, attenu- In conclusion, the present study showed that both cardiorespira-
ated and decreased to non-significant in some [20, 32] but not all tory fitness and muscular endurance are independently associ-
studies [3, 13, 21, 30, 32]. ated with cardiovascular risk factors, whereas no association
The previous cross-sectional studies have measured either max- between maximal strength and cardiovascular risk factors were
imal strength only or a combination of muscular endurance and observed in young adult men. These findings may suggest that in
maximal strength to form a muscular fitness index. Therefore, addition to aerobic training, resistance training, which also
the comparison between the present and earlier findings is induces sufficiently strong training response in the cardiovascu-
rather difficult. The comparison of the previous studies is also lar system, is beneficial for the cardiovascular health. This, how-
challenged by the fact that correction for body composition dif- ever, needs to be further confirmed by more prospective studies
fers between the studies. In some studies, no corrections for and randomized clinical trials.

Vaara JP et al. Associations of Maximal Strength … Int J Sports Med 2014; 35: 356–360
360 Clinical Sciences

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