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448

The effects of high-intensity resistance exercise

on the blood lipid profile and liver function in
hypercholesterolemic hamsters
Fernando Tadeu Trevisan Frajacomo, Marcelo Marcos Piva Demarzo,
Cleverson Rodrigues Fernandes, Flvia Martinello, Jos Alexandre Bachur,
Srgio Akira Uyemura, Srgio Eduardo de Andrade Perez, and Srgio Britto Garcia

Abstract: It is well established that atherogenic dyslipidemia, characterized by high levels of triglycerides (TG), total cholesterol (TC), and low-density lipoprotein (LDL) cholesterol and low levels of high-density lipoprotein (HDL) cholesterol,
constitutes important risk factors for cardiovascular disease. Regular exercise has been associated with a reduced risk for
metabolic diseases. However, studies supporting the concept that resistance exercise is a modifier of blood lipid parameters
are often contradictory. The aim of this study was to investigate the effects of high-intensity resistance exercise on the serum
levels of TG, TC, HDL and non-HDL cholesterol, glucose, and the liver function enzymes alanine aminotransferase (ALT,
EC 2.6.1.2) and aspartate aminotransferase (AST, EC 2.6.1.1) in golden Syrian hamsters (Mesocricetus auratus (Waterhouse, 1839)) fed a hypercholesterolemic diet. Sedentary groups (S) and exercise groups (E) were fed a standard diet (SS
and ES) or a cholesterol-enriched diet (standard plus 1% cholesterol, SC and EC). Resistance exercise was performed by
jumps in the water, carrying a load strapped to the chest, representing 10 maximum repetitions (10 RM, 30 s rest, five days
per week for five weeks). Mean blood sample comparisons were made by ANOVA + Tukey or ANOVA + KruskalWallis
tests (p < 0.05) to compare parametric and nonparametric samples, respectively. There were no differences in blood lipids
between the standard diet groups (SS and ES) (p > 0.05). However, the EC group increased the glucose, non-HDL, and TC
levels in comparison with the ES group. Moreover, the EC group increased the TG levels versus the SC group (p < 0.05).
In addition, the ALT levels were increased only by diet treatment. These findings indicated that high-intensity resistance exercise contributed to dyslipidemia in hamsters fed a hypercholesterolemic diet, whereas liver function enzymes did not differ
in regards to the exercise protocol.
Key words: cholesterol, lipid profile, liver function, resistance exercise, exercise intensity, hypercholesterolemic hamsters.
Rsum : Il est bien admis que la dyslipidmie athrogne est un important facteur de risque de maladie cardiovasculaire;
la dyslipidmie athrogne est caractrise par une forte concentration de triglycrides (TG), de cholestrol total (TC), de lipoprotines de faible densit (LDL) et par une faible concentration de lipoprotines de haute densit (HDL). Daprs des
tudes, la pratique rgulire de lactivit physique est associe la diminution du risque de maladie mtabolique. Pourtant,
les tudes accordant aux exercices contre rsistance la proprit de modifier le bilan lipidique sanguin sont contradictoires.
Cette tude se propose danalyser chez des hamsters (Mesocricetus auratus (Waterhouse, 1839)) sous rgime hypercholestrolmique les effets des exercices contre rsistance de forte intensit sur les concentrations sriques de TG, de TC, de HDL
avec ou sans cholestrol, de glucose et sur les enzymes de la fonction hpatique, lalanine aminotransfrase (ALT, EC
2.6.1.2) et laspartate aminotransfrase (AST, EC 2.6.1.1). Les groupes sdentaires (S) et les groupes soumis lexercice
physique (E) sont aliments au moyen dun rgime standard (SS et ES) ou dun rgime enrichi de cholestrol (standard plus
1 % de cholestrol, SC et EC). Les exercices contre rsistance consistent en des sauts dans leau, dans le transport dune
charge fixe la poitrine, soit lquivalent dun maximum de 10 rptitions (10 RM, 30 s de repos, cinq jours par semaine,
cinq semaines). On utilise une analyse de variance suivie dun test de Tukey pour comparer les valeurs des chantillons paramtriques et une analyse de variance suivie dun test de KruskalWallis pour comparer les chantillons non paramtriques
(p < 0,05). On nobserve aucune diffrence des concentrations sanguines de lipides chez les groupes sous rgime standard
(SS et ES, p > 0,05). En revanche, on observe chez le groupe EC une augmentation du glucose, des HDL sans cholestrol
et de TC comparativement au groupe ES. En outre, on observe chez le groupe EC une plus grande augmentation des TG
comparativement au groupe SC (p < 0,05). De plus, les concentrations de lALT augmentent seulement sous rgime hyperReceived 13 February 2011. Accepted 17 October 2011. Published at www.nrcresearchpress.com/apnm on 12 April 2012.
F.T.T. Frajacomo, C.R. Fernandes, J.A. Bachur, and S.B. Garcia. Department of Pathology and Legal Medicine, Ribeiro Preto
Medical School, University of So Paulo (USP), 3900 Bandeirantes Avenue, 14049 900 Ribeiro Preto, SP, Brazil.
M.M.P. Demarzo. Department of Preventive Medicine, Federal University of So Paulo (UNIFESP), So PauloSP, Brazil.
F. Martinello. Federal University of Santa Catarina (UFSC), Florianpolis, Brazil.
S.A. Uyemura. Department of Clinical, Toxicological, and Food Science Analysis, University of So Paulo (USP), Ribeiro Preto, SP,
Brazil.
S.E.A. Perez. Department of Exercise Physiology, Federal University of So Carlos (UFSCAR), So CarlosSP, Brazil.
Corresponding author: Sergio Britto Garcia (e-mail: sbgarcia@fmrp.usp.br).
Appl. Physiol. Nutr. Metab. 37: 448454 (2012)

doi:10.1139/H2012-008

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cholestrolmique. Daprs ces observations, les exercices contre rsistance de forte intensit contribuent la dyslipidmie
des rats sous rgime hypercholestrolmique; lactivit des enzymes de la fonction hpatique nest pas modifie par des
sances dexercices.
Motscls : cholestrol, profil lipidique, fonction hpatique, exercice contre rsistance, intensit dexercice, hamsters hypercholestrolmiques.
[Traduit par la Rdaction]

Introduction
The core components of dyslipidemia, especially the rise
of triglycerides (TG) levels and the preponderance of lowdensity lipoprotein (LDL) cholesterol and (or) low levels of
high-density lipoprotein (HDL) cholesterol, most likely favor
atherosclerosis and plaque development (Raal 2009). Increased levels of physical activity and fitness are clearly associated with a reduction in the risks associated with metabolic
disorders, and these would be mediated by favorable changes
in the levels of circulating lipoproteins (Leon and Sanchez
2001). However, the optimal type, intensity, frequency, and
duration of exercise training are not yet well known (Canbay
et al. 2007).
Resistance exercise is recommended by the American College of Sports Medicine (ACSM) and the American Heart
Association as an integral part of the exercise program
(ACSM 2009), and recommendations for the use of resistance training as therapy in obesity and metabolic disorders
have recently been provided (Strasser and Schobersberger
2011). However, studies supporting the concept that resistance training is a modifier of serum lipids remains equivocal.
The reduction of the total cholesterol (TC), LDL cholesterol,
and TG levels and elevation of the HDL cholesterol level
were found (Fahlman et al. 2002; Kelley and Kelley 2009).
On the other hand, no improvement of these lipoproteins levels following resistance exercise was reported (Manning et al.
1991; Elliott et al. 2002). Because of the heterogeneity in the
participants characteristics (age, pre- or post-menopausal,
and previous lipidemic status) and the differences of resistance exercise parameters (intensity, volume, and number of
sessions), the influence of resistance exercise on the lipid
and lipoprotein levels remains elusive (Pitsavos et al. 2009).
Resistance exercise intensity has been a parameter frequently
recorded in research (e.g., Kokkinos et al. (1988) and Wallace et al. (1991)). High-intensity resistance exercise was
found to be relevant to the improvement in serum HDL (Hill
et al. 2005). In contrast, other authors suggested that acute
high-intensity resistance exercise was less effective in promoting serum lipid benefits (Lira et al. 2010). Nevertheless,
the previous researchers investigated only healthy subjects,
whereas high-intensity resistance exercise, in addition to hypercholesterolemic diets, remains poorly studied.
Golden Syrian hamsters (Mesocricetus auratus (Waterhouse, 1839)) fed a high-fat diet developed dyslipidemia and
atherosclerotic plaques, similar in many aspects to the human
atherosclerosis (Kasim-Karakas et al. 1996). Moreover, this
animal model presents plasma lipoprotein distribution similar
to that in humans and LDL cholesterol as a major cholesterol
carrier (Auger et al. 2004). In addition, hamsters have demonstrated metabolic response elicited by exercise on the

blood lipid levels similar to that observed in humans (Tsai et

al. 1982). A significant number of studies have been conducted concerning the physical exercise intervention in this
animal model, but most of them used voluntary and low- or
moderate-intensity aerobic exercise protocols (Nichols and
Borer 1987; Tsai and Gong 1987). Hamsters involved in a
voluntary wheel exercise and fed a high-fat diet did not have
their serum TG, TC, and HDL cholesterol levels reduced by
this exercise model (Sandretto and Tsai 1988).
The liver represents an important organ of lipid management, and physical activity may result in transient elevations
of the liver function (Aoi et al. 2004). Although there is no
consensus on what type and volume of exercises could induce changes in the hepatic clinical chemistry parameters or
to what extent, some authors have applied the enzymes aspartate aminotransferase (AST, EC 2.6.1.1) and alanine aminotransferase (ALT, EC 2.6.1.2) as common markers of liver
function in response to exercise (Larson-Meyer et al. 2008;
Sreenivasa Baba et al. 2006), whereas only a few have dealt
with the effects of resistance exercise (Manore et al. 1993;
Levinger et al. 2009).
To address the influence of resistance exercise in addition
to hypercholesterolemic diets, the present study investigated
the effects of the high-intensity resistance exercise protocol
on the serum levels of TC, HDL and non-HDL cholesterol,
glucose, TG, and hepatic liver function enzymes ALT and
AST in hamsters.

Material and methods

Experimental design
Twenty golden Syrian male hamsters were randomly divided into four groups. After they had acclimatized separately
for two weeks in colony cages (five hamsters per cage) at
25 2 C and under a 12 h light 12 h dark cycle, they
were weighed and submitted to the experimental design for
five weeks. Water and food intake were performed ad libitum
in all the groups.
The sedentary group (SS) was fed a standard diet (Guabi
Nutrilabor), and the sedentary + cholesterol group (SC) was
fed a cholesterol-enriched diet (standard diet plus 1% cholesterol). The sedentary groups (SS and SC) were maintained in
colony cages during the entire experiment design and were
not allowed access to wheels or to other kinds of voluntary
exercise apparatus.
The exercise + standard diet group (ES) and the exercise +
cholesterol-enriched group (EC) were submitted to the same
exercise protocol. The animals were weighed at the beginning
and end of the treatment. The study was carried out at the
Department of Pathology of the Ribeiro Preto Medical
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Table 1. Hamster mean body mass before and after exercise protocol and body mass variation.

Body mass (g)

Body mass variation (g)

Initial
Final

SS
1475.38*
1416.29
5.57.08

SC
1326.27
13313.76
0.710.37

ES
1627.58
1598.21
3.79.68

EC
1355.41
13613.87
0.616.31

Note: SS, sedentary + standard diet; SC, sedentary + cholesterol-enriched diet; ES, exercise + standard diet; EC, exercise +
cholesterol-enriched diet. Values are means standard deviations (SD), n = 5.
*SS group statistically different from SC, ES, and EC groups, p < 0.01.

ES group statistically different from SC and EC groups, p < 0.001.

Fig. 1. Effects of cholesterol-enriched diet and high-intensity resistance exercise on blood aspartate aminotransferase (AST) and alanine aminotransferase (ALT) levels. SS, sedentary + standard diet; SC, sedentary + cholesterol-enriched diet; ES, exercise + standard diet; EC, exercise + cholesterol-enriched diet diet. Values are means standard deviations (SD), n = 5. Double asterisks (**) indicate that the SC and EC
groups differ significantly from the SS and ES groups, p < 0.01.

School and followed the University of So Paulo Animal Research and Ethics Committee procedures.
Exercise protocol
The study used the modified protocol of high-intensity resistance exercise training by Cunha et al. (2005). The exercise groups (ES and EC) performed jumping exercises in
water for five weeks, once per day for five days per week.
During the first week, the training groups were adapted to
the water (temperature, 30 2 C) (Harri and Kuusela
1986), and the sessions were performed between 2 and 3 pm
(1400 and 1500 hours). This period consisted of sessions of
weight lifting in water, 18.5 cm in depth, where the animals
had to jump upwards from the bottom of the box, with an incremental number of sets (two to four) and repetitions (five
to 10), with 30 s of rest between each set, carrying a load
representing 10% of the body mass strapped to the chest.
After the adaptation period, hamsters were submitted to
the high-intensity exercise training for four weeks. The load
was adjusted in response to 10 repetitions maximum (10
RM). In this model, failure was considered the incapacity of
the animals to perform jumps in the box. During the first
two weeks of training, the animals performed two sets of 10
jumps per set carrying a load of 15% of their body mass
strapped to the chest, with 30 s of resting between each set.
In the third and fourth weeks of training, the animals performed the same exercise carrying a load of 20% of their
body mass.
Biochemical parameters
Forty-eight hours after the end of the protocol and overnight fasting, the animals were euthanized using a CO2

chamber. The blood samples were obtained by a cardiac

puncture, and the serum was separated and stored at 70 C
until analysis. Biochemical parameters were investigated in
triplicate using an Abbott VP Super System Autoanalyser
(Abbott, Irving, Texas) employing commercial kits (Labtest
Diagnostica, Montes Claros, MG, Brazil). The hepatic function was investigated by the evaluation of the ALT and AST
(Rej and Shaw 1984; Bergmeyer et al. 1986). The blood lipid
profile was evaluated by the determination of the total TC,
HDL cholesterol, glucose, and TG in the serum of the experimental animals. The measurement of the HDL cholesterol in
the serum was carried out after the precipitation of apolipoprotein B (apo-B) containing lipoproteins with dextran sulfate
and magnesium chloride (Warnick et al. 1982). The results
were expressed as non-HDL (VLDL + IDL + LDL) cholesterol instead of LDL cholesterol, because the Friedewald
equation is not applicable to hamsters (Friedewald et al.
1972). Thus, the concentration of lipoprotein (non-HDL)
cholesterol was calculated by subtracting HDL cholesterol
concentrations from the total serum cholesterol.
Statistical analysis
The data were analyzed using the GraphPad Prism V 5.1
(GraphPad Software, Inc., San Diego, California). The normality test was realized by the KolmogorovSmirnov test.
The statistical significance of the differences between the
data means was determined by one-way analysis of variance
(ANOVA) followed by the Tukey post hoc test if values were
parametric and the KruskalWallis test followed by the Dunn
post hoc test if values were nonparametric. A value of p <
0.05 was considered statistically significant. Results are
expressed as means standard deviations (SD), n = 5.
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Frajacomo et al.

451

Fig. 2. Effects of cholesterol-enriched diet and high-intensity resistance exercise on the blood lipid profile. SS, sedentary + standard diet; SC,
sedentary + cholesterol-enriched diet; ES, exercise + standard diet; EC, exercise + cholesterol-enriched diet. Values are means standard
deviations (SD), n = 5. Ampersand (&) indicates that the EC group differs significantly from the SS and ES groups, p < 0.05; single asterisk
(*) indicates that the EC group differs significantly from the ES group, p < 0.05; hatch tag (#) indicates that the SC and EC groups differ
significantly from the SS and ES groups, p < 0.05; and double asterisks (**) indicate that the EC group differs significantly from the SC
group, p < 0.01.

Results
Data of the body mass gain and levels of glucose, AST,
and ALT were normally distributed, and the TG, TC, nonHDL, and HDL levels were non-normally distributed. The
body mass variation did not present a statistically significant
difference among the experimental groups after the adaptation period (p > 0.05) (Table 1). From the measurements of
the serum aminotransferases, the levels of ALT in the groups
on the cholesterol-enriched diet were statistically higher in
comparison with the groups on normal diets (p < 0.01),
whereas no significant difference was detected in the AST
levels (p >0.05) (Fig. 1).
In the serum lipids, the HDL cholesterol was statistically
higher in the groups on a cholesterol-enriched diet (SC and
EC) compared with the groups on the standard diet (SS and
ES) (p < 0.05). The data revealed a significant increase in
the non-HDL cholesterol, TC, and glucose levels in the EC
gruop in relation to the ES group (p < 0.05) (Fig. 2). In addition, exercise treatment elevated the serum TG in the

groups on the cholesterol-enriched diet (EC and SC) (p <

0.01).

Discussion
In the present study, the cholesterol-enriched diet and
high-intensity resistance exercise protocol were conducted to
analyze the serum lipid proteins and liver function in hamsters. In the present results, we observed that the EC group
increased the TC, non-HDL cholesterol, glucose, and TG levels, whereas the HDL and ALT levels were responsive to the
cholesterol-enriched diet only.
The serum aminotransferases ALT and AST are frequently
reported as markers of liver damage (Kew 2000). In our
study, we observed that a cholesterol-enriched diet was associated with a significant increase in the ALT levels, independent of the exercise protocol (Fig. 1). Diets plus 1%
cholesterol resulted in elevated ALT levels in other rodents
as well (Amin and Abd El-Twab 2009). The ALT is considered to be a more specific marker of hepatocellular damage
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452

as it occurs exclusively in the liver, whereas the AST occurs

to some extent in many organs, particularly in the skeletal
muscle (Ozer et al. 2008). Our model did not provide a statistical difference in the AST levels between the groups on the
cholesterol-enriched diet and exercise groups.
Normal liver function is important for the metabolism of
lipids, and it may be influenced by exercise. Although the
majority of the studies have examined the influence of aerobic exercise on the ALT and AST modulation (Botezelli et al.
2010; Sreenivasa Baba et al. 2006), evidence supporting this
observation in the resistance exercise model is sparse; moreover, the liver function enzymes have been reported as
markers of serum muscle damage and may significantly increase after resistance exercise (Levinger et al. 2009; Machado et al. 2010; Pettersson et al. 2008). Our data did not
show statistical differences in these serum aminotransferases
following the high-intensity resistance exercise protocol, independent of the diet administered (Fig. 1). Thus, according
to the body of literature in this area, it is reasonable to consider that a variety of intensities of exercise, muscle damage,
and diet management could have contributed to the variability outcomes in comparison with our data.
The present investigation did not demonstrate statistical
differences of the serum HDL and non-HDL cholesterol, TC,
TG, and glucose levels following the high-intensity resistance
exercise in the standard diet group in comparison with the
sedentary one (Fig. 2). This is consistent with data from
healthy humans after an acute session of high-intensity resistance exercise, which showed lower benefits on serum TG,
LDL, and HDL cholesterol than moderate intensities 72 h
after the exercise bout (Lira et al. 2010). In general, highintensity resistance exercise and training have demonstrated
little effect on chronic lipid profile in healthy humans (Hill
et al. 2005; Kokkinos et al. 1988). Nevertheless, in addition
to the cholesterol-enriched diet, our exercise protocol elevated the TC, non-HDL cholesterol, and glucose serum levels in comparison with the ES group (p < 0.05);
furthermore, the TG serum levels were elevated in comparison with the SC group (p < 0.01). In fact, these results
would indicate a greater risk for cardiovascular disease in
hamsters (Dillard et al. 2010) and humans (Chapman et al.
2011; Cziraky et al. 2008). However, in the context of the
resistance exercise, dietary and serum cholesterol may act as
potential contributors to skeletal muscle adaptation in response to exercise training (Riechman et al. 2007). Interestingly, after eccentric exercise contraction, a particular model
of resistance exercise associated with microtears, inflammation, and soreness, a large turnover and rapid metabolism of
cholesterol was observed (Riechman et al. 2009). Unfortunately, because of the exiguity of studies that evaluated
muscle integrity after the water jumping exercise associated
with the cholesterol-enriched diet, it is difficult to correlate
the mechanisms responsible for these alterations in the EC
group. We suggest that more studies associating high-intensity
resistance exercise, cholesterol-enriched diets, and chronic
lipid metabolism and their relationships with cardiovascular
diseases should be performed.
Although we consider these findings important and recent
in this area, there were some limitations in the present investigation. The strength of the present findings is limited by the
small samples of hamsters per group, which may justify the

Appl. Physiol. Nutr. Metab. Vol. 37, 2012

lack of statistical significance in some analysis, and the results should be carefully interpreted. Another major limitation of our study was the absence of food intake recorded
following the experimental period, although a previous research reported no difference in food intake with a similar
cholesterol diet in hamsters (Martinello et al. 2006). Thus,
the lack of significant change in body mass gain among all
the groups suggests that the absence of food intake recorded
does not have an appreciable influence on the results.
Here, we observed that high-intensity resistance training,
in addition to a cholesterol-enriched diet, elevated the serum
TG, glucose, non-HDL, and TC levels after the experiment.
The ALT blood levels were only elevated by the cholesterolenriched diet. Whether such changes would alter atherosclerotic risk in this population remains to be shown. Therefore,
in spite of some limitations in the current investigation, this
model may encourage further studies to address the mechanisms involved in the relationship between resistance exercise
adaptation, muscle metabolism, and cholesterol-enriched diet
on cardiovascular diseases.

Acknowledgements
The authors thank the Laboratory of Clinical Analysis at
the Department of Clinical, Toxicological, and Food Science
Analysis, University of So Paulo Ribeiro Preto (Brazil)
for providing the use of the Abbott VP Super System Autoanalyser. We also thank Rosngela Orlandim Lopes for technical assistance. Financial support was provided by
Coordenao de Aperfeioamento de Pessoal de Nvel Superior (CAPES Brazil) and by the University of So Paulo.

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