RESEARCH Open Access

Exercise and spirulina control non-alcoholic

hepatic steatosis and lipid profile in diabetic
Wistar rats
Leandro P Moura
*
, Guilherme M Puga, Wladimir R Beck, Inaian P Teixeira, Ana Carolina Ghezzi, Glucio A Silva and
Maria Alice R Mello
Abstract
Background: Diabetes mellitus is associated with metabolic dysfunctions, including alterations in circulating lipid
levels and fat tissue accumulation, which causes, among other pathologies, non-alcoholic fatty liver disease
(NAFLD).
Aim of the study: The objective of this study was to analyse the effects of physical exercise and spirulina intake
on the control of NAFLD in diabetic Wistar rats.
Methods: Diabetes was induced in the animals through intravenous administration of alloxan. The rats were
divided into four groups: Diabetic Control (DC) - diabetic rats fed with a control diet and no physical exercise;
Diabetic Spirulina (DS) - diabetic rats fed with a diet that included spirulina; Diabetic Spirulina and Exercise (DSE) -
diabetic rats fed with a diet that included Spirulina and that exercised; and Diabetic Exercise (DE) - diabetic rats fed
with a control diet and that exercised.
Results: The groups DS, DSE, and DE presented lower plasma concentrations of LDL cholesterol than DC, as well
as lower levels of total liver lipids in groups DS, DSE, and DE in comparison to DC.
Conclusion: Thus, spirulina appears to be effective in reducing total circulating levels of LDL-cholesterol and
hepatic lipids, alone or in conjunction with physical exercise in diabetic rats.
Introduction
Type 1 diabetes (DM-1), is an autoimmune illness that
primarily affects young people. Because patients with
type 1 diabetes do not produce sufficient quantities of
insulin, they are dependent on exogenous insulin to
maintain blood glucose at normal levels. In turn, type 2
diabetes (DM-2) occurs more slowly and later in life
(after forty years of age) than type 1.
The complications associated with diabetes are severe.
The illness is one of the main causes of blindness, kid-
ney disease, macrovascular disease and atherosclerosis,
liver disease and a variety of debilitating neuropathies
that diminish the quality of life and life expectancy of
the patients [1]. The imbalance of the circulating lipid
profile is a consequence of diabetes mellitus [2]. Accord-
ing to Carew et al. [3], the imbalance in the concentra-
tion of serum lipoproteins can promote the movement
of cholesterol from peripheral tissues to the liver for
catabolic excretion. In cases where this transference to
the liver is high and the catabolic level is low, fat can
accumulate in this organ, causing non-alcoholic fatty
liver disease (NAFLD). Furthermore, chronically high
concentrations of serum lipids associated with a low
level of catabolism can create the same condition. This
illness is characterised by the presence of large depots
of fat in the liver and the absence of inflammatory pro-
cesses and is known as hepatic steatosis [4].
In addition to dietary control, physical exercise has
been heavily used as a non-pharmaceutical treatment
for the control and reduction in abnormal levels of cir-
culating lipids and glucose in individuals with metabolic
dysfunctions such as diabetes [5,6].
* Correspondence: [email protected]
So Paulo State University Jlio de Mesquita Filho. Department of Physical
Education. Institute of Biosciences. Laboratory of nutrition, metabolism and
exercise. Av 24A, 1.515, Bela Vista - 13.506-900 - Rio Claro, SP, Brazil
Moura et al. Lipids in Health and Disease 2011, 10:77
http://www.lipidworld.com/content/10/1/77
2011 Moura et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
From this perspective, functional foods have been used
for the control of these metabolic dysfunctions. Some
authors have demonstrated that spirulina intake can
regulate cholesterol, increase the antioxidant capacity,
and improve insulin resistance and the uptake of
glucose [7-9].
Spirulina is a helical blue-green alga, which contains
65 to 70% protein [10,11]. Although it has a slightly
reduced digestibility [12], it appears to be a good food
source of protein. In addition, some studies show that
spirulina has beneficial effects on the treatment of mal-
nutrition [13,14] and on other pathologies such as obe-
sity [13,15], hypercholesterolaemia [13,11], arterial
hypertension [13,16,17] and diabetes mellitus [13].
In agreement with Hosoyamada et al. [9], the water-
soluble fraction of spirulina is effective in diminishing
serum glucose levels in fasting rats [12] due to phyco-
cyanin, which is capable of reducing concentrations of
circulating glucose [13]. According to studies by Layam
and Reddy [18], when this alga is administered at a con-
centration of 15 mg/kg body weight, it can raise serum
insulin levels in DM-1 rats.
Given the difficulties encountered in studies that
involve hepatic steatosis in human subjects, several stu-
dies have been performed using animal subjects, which
permits researchers strict control of nutrition and
environment and also the analysis of specific tissues,
such as hepatic and myocardial tissues. Thus, the
objective of the present study was to verify the effects
spirulina intake and of swimming training on the lipid
profile, in hepatic steatosis and on the accumulation of
lipids in myocardial and skeletal muscle of diabetic
Wistar rats.
Materials and methods
Animals and Treatment
The study used young Wistar rats (60 days old), which
came from the Central Vivarium (Biotrio Central) of
UNESPA - at the Botucatu Campus and were main-
tained in the vivarium of the biodynamic laboratory of
the Department of Physical Education, Biosciences
Institute of UNESP - Rio Claro Campus. The animals
were housed in polyethylene cages (five animals per
cage) and kept at a controlled room temperature of 23
1C, with a photoperiod of 12 hours of light/12
hours of dark with food and water ad libitum. The
experiment was conducted in accordance with current
Brazilian legislation and standards of the Brazilian Col-
lege of Animal Experimentation (Colgio Brasileiro de
Experimentao Animal-COBEA). All standards were
adhered to rigorously. The use of animals in this study
was approved by the ethics committee at the Bios-
ciences Institute at UNESP - Rio Claro (protocol 5111
of 08/20/09).
Induction of Diabetes
Experimental diabetes was induced by administration of
alloxan monohydrate (Sigma, 32 mg.kg
-1
of body weight)
dissolved in citrate 0.01 M, pH 4.5, injected into the
penile vein. After this procedure, the animals were
returned to their cages and received, in the first 24
hours post-alloxan, a solution of water and glucose
(15%), in addition to feed [19]. Two weeks after admin-
istration of the drug, the blood glucose level of the ani-
mals was tested for evidence of a diabetic state. The
animals that had a blood glucose level equal to or
greater than 190 mg.dL
-1
were included in the study.
Experiment Design
After the induction of type 1 diabetes, the animals were
randomly distributed into four groups (10 per group):
Diabetic Control (DC) - composed of alloxan diabetic
rats that were given a control diet and no exercise; Dia-
betic Spirulina (DS) - composed of alloxan diabetic rats
fed with a diet that included spirulina and no exercise;
Diabetic Spirulina and Exercise (DSE) - composed of
alloxan diabetic rats fed with a diet that included spiru-
lina and that exercised; Diabetic Exercise (DE) - com-
posed of alloxan diabetic rats fed with a control diet and
that exercised.
Diets
Following the recommendations of the American Insti-
tute of Nutrition AIN-M93 [20], isocaloric and semi-
purified diets were utilised; the control diet for the ani-
mals in the control (DC) and exercise (DE) groups con-
tained 17% casein protein, and the rats in the spirulina
groups (DS and DSE) were fed with a diet containing
17% spirulina protein. The control diet was composed
of the following (%): corn starch = 39.7, dextrin = 13.2,
sucrose = 10, soy oil = 7, microcellulose = 5, a mixture
of six minerals = 3.5, and a mixture of vitamins = 1. A
detailed description of the mineral and vitamin mixtures
can be found in Reeves et al. [20]. The spirulina diet
contained the same quantities of carbohydrates and
lipids as the control diet. There were adjustments made
only in the contents of the six minerals, the vitamins,
and the fibres, taking into account the levels of these
elements already in the spirulina, so that the recom-
mendations of AIN-M93 for these nutrients would be
maintained [21].
Adaptation to the liquid medium and exercise protocol
In the first week, the animals were put into contact with
shallow water for adaptation to the liquid medium.
From the second week, they had swimming exercise
with increasing amounts of time. The training sessions
were held in collective tanks with a constant water tem-
perature of 31 1C, for 1 hour/day, 5 days/week, for a
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total period of 44 days. During the exercise, a backpack
was attached to the thorax of the animal with a load
equivalent to 3.5% of body weight. This protocol was
selected to represent aerobic exercise below the lactate
threshold for diabetic rats [22].
Assessments of animals prior to their sacrifice
During the entire experimental period, all the animals
had their body mass, water and food intake registered.
The results were analysed calculating the area under the
curves in the variations of body mass and food intake
over time using the trapezoidal rule [23].
Assessments of animals after their sacrifice
At the end of the experimental period, 48 hours after
the final in vivo evaluations, at feed and rest condi-
tions, all the rats were anaesthetised in a CO
2
chamber
until they were sedated. They were then exsanguinated,
and their blood was collected. The blood was centri-
fuged at 3000 rpm for 15 minutes, and analyses of glu-
cose, total cholesterol, triglycerides, HDL cholesterol,
LDL cholesterol, total protein, and albumin were per-
formed using samples of supernatant serum, through
colourimetric methods with commercial colourimetry
test kits (Laborlab

, Guarulhos - SP/Brazil). Free fatty

acid (FFA) were also analysed according to the Regow
method [24], and insulin was measured by radioimmu-
noassay [25].
Samples of the left ventricle, the liver, and the gastro-
cnemius muscle were taken to determine the concentra-
tions of triglycerides and total lipids. The samples were
placed into tubes containing 0.1% Triton X-100. They
were then homogenised with a Polytron

for 20 seconds
at a maximum velocity. After this procedure, the sam-
ples were centrifuged at 4.000 rpm for 10 minutes. The
supernatant was extracted to determine the triglycerides
and total lipid using spectrophotometry with a commer-
cial kit (Laborlab

, Guarulhos - SP/Brazil).
Statistical Analysis
The results are expressed as means and standard devia-
tions. After checking the data for normalcy using the
Shapiro-Wilk test, the values of the lipid profile, plasma
proteins, adipose tissue proteins, areas under the curve
of variations in body mass and the intake of food and
water during the experiment were compared between
the groups using analysis of variance - one way ANOVA
with Tukeys post-hoc test. The adopted significance
level was p < 0.05.
Results
The results of body mass in each group are shown in
Figure 1. All groups had significantly reduced body
mass by the end of the 44 days of training in relation to
pre-intervention values as indicated by the area under
the curve of body mass over time (Figure 1-a). Further-
more, the statistical analysis did not show a significant
difference between the groups regarding the change ()
in body mass (final value of body mass - initial value of
body mass) during the experiment, as shown in Figure
1-b. There was also no difference between the groups
when the values of the area under the curve of body
mass were compared, as demonstrated in Figure 1-c.
The results of water intake in each group are illu-
strated in Figure 2-a. There was no statistical difference
between the areas under the curve of water intake over
time (Figure 2-b) when comparing all groups. The sta-
tistical analysis also did not show a significant difference
between areas under the curve of food intake when
comparing all groups (Figures 2-c and 2-d).
The results of serum concentrations of glucose, insu-
lin, total, HDL and LDL cholesterol, triglycerides, FFA,
total proteins, and plasma albumin of all groups are pre-
sented in Table 1. For the concentrations of serum insu-
lin, the DS group had a significantly lower value when
compared to the DC, DE, and DSE groups. The statisti-
cal analysis did not show differences in concentrations
of glucose, total cholesterol, triglycerides, FFA, or total
proteins in the groups studied.
The concentrations of LDL cholesterol were 34 and
42% less in the DS and DSE groups, respectively, in rela-
tion to the DC group. The HDL cholesterol levels were
20% lower in the DSE group in relation to the DC
group. Furthermore, the concentration of albumin was
17% lower in the DSE group in relation to the DC
group.
The results of the tissue concentrations of lipids are
presented for all groups in Table 2. The statistical analy-
sis did not show a significant difference in triglyceride
concentrations in muscular tissue or in the left ventricle
myocardial groups but did show that the concentration
of hepatic triglycerides was 43% less in the DS group in
relation to the DC group. In turn, the concentrations of
total hepatic lipids were 46, 44 and 43% lower in rela-
tion to the DC group for the DS, DSE and DE groups,
respectively.
Discussion
This study aimed at assessing the effects of spirulina
intake and physical exercise on circulating and tissue
lipid levels (hepatic, myocardial, and skeletal muscle) in
diabetic Wistar rats. The principal finding of our study
was that spirulina in the diet of these rats resulted in an
attenuation of fatty deposits in the liver as well as lower
plasma levels of LDL cholesterol in comparison to the
diabetic control group that did not receive treatment.
In fact, the literature has shown conflicting results in
studies including a diet with spirulina and exercise. One
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of the first studies with rats consuming spirulina
showed a reduction in total cholesterol levels when
examining the lipid profile [26]. Since then, various stu-
dies have been conducted using animal [17,27,28] and
human models [29,30].
In relation to the intake of water and food, the statisti-
cal analysis showed that there was no significant differ-
ence between groups (Figure 2). Furthermore, total
protein concentrations and serum albumin that can be
used as measures of the nutritional and hydration states
of animals showed values quite similar to those already
reported by other authors that also study active and
sedentary diabetic Wistar rats [31].
Using an experimental model, Kato et al. [27] sub-
mitted rats to a diet rich in cholesterol with and without
spirulina supplementation. In this study, the authors
observed an increase in total cholesterol levels overall,
LDL + VLDL cholesterol and phospholipids in the
serum of the group that did not ingest spirulina. How-
ever, there was a significant reduction in the levels of
these cholesterol fractions when the animals were sup-
plemented with 16% spirulina.
Iwata et al. [17] observed that spirulina supplementa-
tion inhibited the increase of HDL - cholesterol,
triglycerides, and phospholipids in the plasma. On the
other hand, there was no statistical significance observed
between the control group and the groups supplemen-
ted with spirulina when lipid levels in the liver were
compared. Furthermore, the authors reported an
increase in lipoprotein lipase enzyme activity in the ani-
mals that received spirulina supplementation.
The results found in the literature on the relationship
between lipid profiles and spirulina intake need more
controlled studies. Recently Cheong et al. [32] affirmed
that the anti-hypercholesterolaemia mechanisms of spir-
ulina are still not well understood, although some
authors suggest that the addition of this alga into the
diet diminishes the intestinal absorption of cholesterol
as well as the re-absorption of bile acids in the ileum.
Thus, they suggest that spirulina can be considered a
functional food capable of reducing the levels of choles-
terol and consequently preventing atherosclerosis.
Our results seem to corroborate the finding of Kato et
al. [27], who show a reduction in the levels of serum
cholesterol in animals supplemented with spirulina.
However, the unexpected finding in our data was the
reduction of HDL cholesterol found in the DSE group
in relation to the DC group. The literature still contains
-2000
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*
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w
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(
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a b
c
Figure 1 Mean and standard error of body mass - a; the difference between body mass pre- and post-intervention ( = variation of mass in
relation to initial mass over time) - b; area under the curve of body mass over time of the body mass - c. DC - control group; DS - group with
spirulina intake and without exercise; DSE - group with spirulina intake and with exercise; and DE - group without intake of spirulina and with
exercise (10 animals/group).
Moura et al. Lipids in Health and Disease 2011, 10:77
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conflicting findings in relation to this fraction of choles-
terol and spirulina supplementation. Iwata et al. [17]
suggest that spirulina can inhibit or augment HDL cho-
lesterol, and it seems that this variable does not have a
determined variable according to the modifications
caused by the action of spirulina.
Corroborating the work of Bl-Castillo et al. [33], who
observed that the administration of spirulina prevented
an increase of total hepatic lipids (40%), our study found
a positive effect from both exercise and a diet including
spirulina when we verified the reduction in total lipids
in hepatic tissue (in the DS, DSE and DE groups in
0
20
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Figure 2 Mean and standard error of water consumption (a) and area under the curve (b) of all groups. Median values of food
consumption (c) and the area under the curve (d) of all groups. DC - control group; DS - group with spirulina intake and without exercise; DSE -
group with spirulina intake and with exercise; and DE - group without intake of spirulina and with exercise (10 animals/group).
Table 1 Serum analysis at the end of the experiment.
DC DS DSE DE
Total Cholesterol (mg.dL
-1
) 108.8 (9.8) 105.5 (4.9) 94.3 (6.2) 91.2 (4.0)
HDL - Cholesterol (mg.dL
-1
) 19.8 (0.8) 17.7 (0.7) 15.7 (1.0)* 18.4 (0.7)
LDL - Cholesterol (mg.dL
-1
) 64.0 (7.3) 42.2 (5.7)* 37.4 (3.9)* 52.2 (3.8)
Triglycerides (mg.dL
-1
) 105.6 (9.9) 237.2 (39.9) 237.8 (46.4) 112.7 (22.2)
Free Fatty Acids (mg.dL
-1
) 0.66 (0.05) 0.66 (0.06) 0.62 (0.04) 0.67 (0.04)
Albumin (mg%) 2.61 (0.06) 2.42 (0.02) 2.28 (0.14)* 2.56 (0.06)
Total Proteins (mg%) 7.66 (0.36) 7.19 (0.11) 7.34 (0.32) 7.47 (0.19)
Glucose (mg.dL
-1
) 303.20 (70.69) 289.25 (106.65) 248.88 (84.92) 275.40 (90.90)
Insulin (U.mL
-1
) 1.64 (0.21) 0.43 (0.21)* 12.69 (3.24) 9.73 3.68
Results expressed with means and (standard errors) of 10 animals/group. DC: Diabetic Control, DS: Diabetic Spirulina, DSE: Diabetic Spirulina Exercise and DE:
Diabetic Exercise. Statistical Difference (ANOVA p < 0.05), *= different from DC.
Moura et al. Lipids in Health and Disease 2011, 10:77
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comparison to the DC group) and the triglycerides of
these same tissues (the DS group in comparison to the
DC group).
According to the results found in the circulating lipid
profile, it is possible to observe that the association between
the effects of diet with spirulina and exercise seem to cause
major changes. When analysed from this perspective, the
HDL and LDL cholesterols were different for the DSE
group in relation to the DC group. However, when we look
at the specific effect of one of the conditions, the results
point to the possibility that only spirulina causes modifica-
tions, causing a statistical difference in the LDL cholesterol.
We understand that the positive effects found for hepatic
and plasma levels are very important when we analyse lipid
metabolism, and that spirulina, mainly when associated
with exercise, seems to be an agent capable of causing
interesting modifications in this metabolism.
By analysing the study of Moura et al. [34], we verified
that the rats from the same breed used here (Wistar),
non-diabetic and maintained with a balanced diet
showed concentrations of total hepatic tissue lipids of
3.5 0.4 mg% for sedentary animals and of 3.5 0.5
mg% for water-exercised animals. Compared with these
data, we report results that were approximately 117, 24,
21 and 18% higher in the DC, DS, DSE and DE groups,
respectively. Thus, we can assert that hepatic steatosis
was induced in the DC group and present evidence that
the intervention of spirulina and/or exercise seems to
reduce the accumulation of total hepatic lipids in dia-
betic rats, thereby attenuating hepatic steatosis.
Conclusion
Based on our results, we conclude that spirulina intake
can provide lower levels of circulating LDL cholesterol
in comparison to aerobic training in diabetic Wistar
rats. Furthermore, both spirulina intake and physical
exercise cause an improvement in hepatic steatosis in
these animals.
Conflicts of interest
The authors declare that they have no competing
interests.
List of abbreviations
DM-1: type 1 diabetes mellitus; DM-2: type 2 diabetes mellitus; NAFLD: non-
alcoholic fatty liver disease; FFA: free fat acids.
Acknowledgements
The authors would like to thank the technicians at the Biodynamic
Laboratory of the Physical Education Department at UNESP Campus Rio
Claro for their indispensible support, Clarice Sibuya and Jos Roberto
Rodrigues, and the National Council of Scientific and Technological
Development - CNPq, the Foundation for Research Support of So Paulo -
FAPESP for the financial support and FUNDUNESP. We also thank Corn
Products Brasil

for the donation of the dietary materials used in this

experiment.
Authors contributions
All authors was responsible for the experimental design, data collection,
statistical analysis and preparation of the manuscript. All authors worked
read and approved the final manuscript.
Received: 14 March 2011 Accepted: 15 May 2011
Published: 15 May 2011
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Table 2 Tissue lipids analyses at the end of the
experiment.
DC DS DSE DE
Liver
Total Lipids (mg
%)
07.61
(1.52)
04.15
(0.17)*
04.24
(0.29)*
04.36
(0.49)*
Triglycerides (mg
%)
18.52
(3.87)
10.59
(1.05)*
11.11
(1.32)
12.12
(1.94)
Gastrocnemius
Muscle
Triglycerides (mg
%)
12.04
(1.60)
08.82
(0.95)
08.38
(0.84)
09.17
(0.98)
Left Ventricle
Triglycerides (mg
%)
5.95 (0.59) 07.07
(0.67)
06.27
(0.59)
6.43 (0.70)
Results expressed with means and (standard errors) of 10 animals/group. DC:
Diabetic Control, DS: Diabetic Spirulina, DSE: Diabetic Spirulina Exercise and
DE: Diabetic Exercise. Statistical Difference (ANOVA p < 0.05), *= different
from DC.
Moura et al. Lipids in Health and Disease 2011, 10:77
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doi:10.1186/1476-511X-10-77
Cite this article as: Moura et al.: Exercise and spirulina control non-
alcoholic hepatic steatosis and lipid profile in diabetic Wistar rats. Lipids
in Health and Disease 2011 10:77.
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